Skip to main content

Advertisement

SpringerLink
Log in

Immunogenicity of two Echinococcus granulosus antigens EgA31 and EgTrp in mice

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Here, we investigate in mice the immunogenicity of two antigens EgA31 and EgTrp which are expressed by the larval stage of Echinococcus granulosus. These recombinant proteins were used alone or as a mixture (EgA31–EgTrp) to immunize BALB/c mice. By flow cytometry, we have shown that the ratio CD4+/CD8+ of splenocytes were significantly higher in the antigen-immunized groups. The specific antibody in the sera and cytokine producing splenocytes was evaluated by enzyme-linked immunosorbent assay. EgA31, EgTrp or EgA31–EgTrp elicited high antibody titer of IgG and IgA. Among IgG isotypes, IgG1 was predominant for each antigen tested alone or combined. The production of IL-12, IFN-γ, IL-10 and IL-6 cytokines was significantly higher in mice immunized with recombinant proteins. Our results suggest that, in BALB/c mice, a mixed Th1/Th2, response to EgA31, EgTrp and EgA31–EgTrp is obtained. The use of both antigens separately or in combination as candidate vaccine proteins is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Briere F, Servet-Delprat C, Bridon JM, Saint-Remy JM, Banchereau J (1994) Human interleukin 10 induces naive surface immunoglobulin D+ (sIgD+) B cells to secrete IgG1 and IgG3. J Exp Med 179:757–762

    Google Scholar 

  • Carol H, Nieto A (1998) A mucosal IgA response, but no systemic antibody response, is evoked by intranasal immunisation of dogs with Echinococcus granulosus surface antigens iscoms. Vet Immunol Immunopathol 65:29–41

    Google Scholar 

  • Carol H, Nieto A, Villacres-Eriksson M, Morein B (1997) Intranasal immunization of mice with Echinococcus granulosus surface antigens iscoms evokes a strong immune response, biased towards glucidic epitopes. Parasite Immunol 19:197–205

    Google Scholar 

  • Cervi L, Borgonovo J, Egea M, Chiapello L, Masih D (2004) Immunization of rats against Fasciola hepatica using crude antigens conjugated with Freund’s adjuvant or oligodeoxynucleotides. Vet Immunol Immunopathol 97:97–104

    Google Scholar 

  • Chabalgoity JA, Harrison JA, Esteves A, Demarco de Hormaeche R, Ehrlich R, Khan CM, Hormaeche CE (1997) Expression and immunogenicity of an Echinococcus granulosus fatty acid-binding protein in live attenuated Salmonella vaccine strains. Infect Immun 65:2402–2412

    Google Scholar 

  • Chow C, Gauci CG, Cowman AF, Lightowlers MW (2001) A gene family expressing a host-protective antigen of Echinococcus granulosus. Mol Biochem Parasitol 118:83–88

    Google Scholar 

  • Cox JC, Coulter AR (1997) Adjuvants—a classification and review of their modes of action. Vaccine 15:248–256

    Google Scholar 

  • Dematteis S, Baz A, Rottenberg M, Fernandez C, Orn A, Nieto A (1999) Antibody and Th1/Th2-type responses in BALB/c mice inoculated with live or dead Echinococcus granulosus protoscoleces. Parasite Immunol 21:19–26

    Google Scholar 

  • Esteves A, Senorale M, Ehrlich R (2003) A tropomyosin gene is differentially expressed in the larval stage of Echinococcus granulosus. Parasitol Res 89:501–502

    Google Scholar 

  • Ferragut G, Nieto A (1996) Antibody response of Echinococcus granulosus infected mice: recognition of glucidic and peptidic epitopes and lack of avidity maturation. Parasite Immunol 18:393–402

    Google Scholar 

  • Finkelman FD, Holmes J, Katona IM, Urban JF, Beckmann MP, Park LS, Schooley KA, Coffman RL, Mosmann TR, Paul WE (1990) Lymphokine control of in vivo immunoglobulin isotype selection. Annu Rev Immunol 8:303–333

    Article  CAS  PubMed  Google Scholar 

  • Flanigan TP, King CH, Lett RR, Nanduri J and Mahmoud AA (1989) Induction of resistance to Schistosoma mansoni infection in mice by purified parasite paramyosin. J Clin Invest 83:1010–1014

    Google Scholar 

  • Fraize M, Sarciron ME, Saboulard D, Azzouz S, Debard AL, Bosquet G, Petavy AF (2004) An in vitro model to evaluate the cytokine response in Echinococcus infections. Parasitol Res 9:506–512

    Google Scholar 

  • Fu Y, Martinez C, Chalar C, Craig PS, Ehrlich R, Petavy AF, Bosquet G (1999) A new potent antigen from Echinococcus granulosus associated with muscles and tegument. Mol Biochem Parasitol 102:43–52

    Google Scholar 

  • Fu Y, Saint-Andre Marchal I, Marchal T, Bosquet G, Petavy AF (2000) Cellular immune response of lymph nodes from dogs following the intradermal injection of a recombinant antigen corresponding to a 66 kDa protein of Echinococcus granulosus. Vet Immunol Immunopathol 74:195–208

    Google Scholar 

  • Gupta RK (1998) Aluminum compounds as vaccine adjuvants. Adv Drug Deliv Rev 32:155–172

    Google Scholar 

  • Haralabidis S, Karagouni E, Frydas S, Dotsika E (1995) Immunoglobulin and cytokine profile in murine secondary hydatidosis. Parasite Immunol 17:625–630

    Google Scholar 

  • Heath DD (1995) Immunology of Echinococcus infections. In: Thompson RCA, Lymbery AJ (eds) Echinococcus and hydatid disease. CAB International, UK, pp 183–199

    Google Scholar 

  • Jankovic D, Sher A, Yap G (2001) Th1/Th2 effector choice in parasitic infection: decision making by committee. Curr Opin Immunol 13:403–409

    Google Scholar 

  • Janssen D, Osuna A, Lazuen J, de Rycke PH (1992) Comparative cytotoxicity of secondary hydatid cysts, protoscoleces, and in vitro developed microcysts of Echinococcus granulosus. J Helminthol 66:124–131

    Google Scholar 

  • Jenkins RE, Taylor MJ, Gilvary NJ, Bianco AE (1998) Tropomyosin implicated in host protective responses to microfilariae in onchocerciasis. Proc Natl Acad Sci USA 95:7550–7555

    Google Scholar 

  • Kuribayashi K, Tsukiyama M, Takenaka T (1997) Secretion patterns of Th1- and Th2-type cytokines in immune deviation caused by dendritic cells. Int Arch Allergy Immunol 114:30–37

    Google Scholar 

  • Li BW, Chandrashekar R, Weil GJ (1993) Vaccination with recombinant filarial paramyosin induces partial immunity to Brugia malayi infection in jirds. J Immunol 150:1881–1885

    Google Scholar 

  • Liu D, Lightowlers MW, Rickard MD (1992) Examination of murine antibody response to secondary hydatidosis using ELISA and immunoelectrophoresis. Parasite Immunol 14:239–248

    Google Scholar 

  • Macy DW (1997) Vaccine adjuvants. Semin Vet Med Surg (Small Anim) 12:206–211

    Google Scholar 

  • Mosmann TR, Coffman RL (1989) Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 7:145–173

    Article  CAS  PubMed  Google Scholar 

  • Nanduri J, Kazura JW (1989) Paramyosin-enhanced clearance of Brugia malayi microfilaremia in mice. J Immunol 143:3359–3363

    Google Scholar 

  • Nara T, Matsumoto N, Janecharut T, Matsuda H, Yamamoto K, Irimura T, Nakamura K, Aikawa M, Oswald I, Sher A et al (1994) Demonstration of the target molecule of a protective IgE antibody in secretory glands of Schistosoma japonicum larvae. Int Immunol 6:963–971

    Google Scholar 

  • O’Garra A (1998) Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8:275–283

    Google Scholar 

  • Ortona E, Margutti P, Vaccari S, Rigano R, Profumo E, Buttari B, Chersi A, Teggi A, Siracusano A (2001) Elongation factor 1 beta/delta of Echinococcus granulosus and allergic manifestations in human cystic echinococcosis. Clin Exp Immunol 125:110–116

    Google Scholar 

  • Ortona E, Vaccari S, Margutti P, Delunardo F, Rigano R, Profumo E, Buttari B, Rasool O, Teggi A, Siracusano A (2002) Immunological characterization of Echinococcus granulosus cyclophilin, an allergen reactive with IgE and IgG4 from patients with cystic echinococcosis. Clin Exp Immunol 128:124–130

    Google Scholar 

  • Ortona E, Margutti P, Delunardo F, Vaccari S, Rigano R, Profumo E, Buttari B, Teggi A, Siracusano A (2003a) Molecular and immunological characterization of the C-terminal region of a new Echinococcus granulosus Heat Shock Protein 70. Parasite Immunol 25:119–126

    Google Scholar 

  • Ortona E, Rigano R, Buttari B, Delunardo F, Ioppolo S, Margutti P, Profumo E, Teggi A, Vaccari S, Siracusano A (2003b) An update on immunodiagnosis of cystic echinococcosis. Acta Trop 85:165–171

    Google Scholar 

  • Reed SG, Coler RN, Campos-Neto A (2003) Development of a leishmaniasis vaccine: the importance of MPL. Expert Rev Vaccines 2:239–252

    Google Scholar 

  • Rigano R, Profumo E, Ioppolo S, Notargiacomo S, Ortona E, Teggi A, Siracusano A (1995) Immunological markers indicating the effectiveness of pharmacological treatment in human hydatid disease. Clin Exp Immunol 102:281–285

    Google Scholar 

  • Rigano R, Profumo E, Bruschi F, Carulli G, Azzara A, Ioppolo S, Buttari B, Ortona E, Margutti P, Teggi A, Siracusano A (2001) Modulation of human immune response by Echinococcus granulosus antigen B and its possible role in evading host defenses. Infect Immun 69:288–296

    Google Scholar 

  • Rincon M, Anguita J, Nakamura T, Fikrig E, Flavell RA (1997) Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J Exp Med 185:461–469

    Google Scholar 

  • Saboulard D, Lahmar S, Petavy AF, Bosquet G (2003) The Echinococcus granulosus antigen EgA31: localization during development and immunogenic properties. Parasite Immunol 25:489:501

    Google Scholar 

  • Seder RA, Paul WE (1994) Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu Rev Immunol 12:635–673

    Google Scholar 

  • Severi MA, Ferragut G, Nieto A (1997) Antibody response of Echinococcus granulosus infected mice: protoscolex specific response during infection is associated with decreasing specific IgG1/IgG3 ratio as well as decreasing avidity. Parasite Immunol 19:545–552

    Google Scholar 

  • Sher A, Coffman RL (1992) Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annu Rev Immunol 10:385–409

    Google Scholar 

  • Siles-Lucas M, Merli M, Mackenstedt U, Gottstein B (2003) The Echinococcus multilocularis 14-3-3 protein protects mice against primary but not secondary alveolar echinococcosis. Vaccine 21:431–439

    Google Scholar 

  • Stevens TL, Bossie A, Sanders VM, Fernandez-Botran R, Coffman RL, Mosmann TR, Vitetta ES (1988) Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334:255–258

    Google Scholar 

  • Taylor MJ, Jenkins RE, Bianco AE (1996) Protective immunity induced by vaccination with Onchocerca volvulus tropomyosin in rodents. Parasite Immunol 18:219–225

    Google Scholar 

  • Tewary P, Sukumaran B, Saxena S, Madhubala R (2004) Immunostimulatory oligodeoxynucleotides are potent enhancers of protective immunity in mice immunized with recombinant ORFF leishmanial antigen. Vaccine 22:3053–3060

    Google Scholar 

  • Vuitton DA (2003) The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Trop 85:119–132

    Google Scholar 

  • Woollard DJ, Gauci CG, Heath DD, Lightowlers MW (2000) Protection against hydatid disease induced with the EG95 vaccine is associated with conformational epitopes. Vaccine 19:498–507

    Google Scholar 

Download references

Acknowledgements

This work was supported by INCO-MED (ICFP599A3PR01) 2000–2004. The authors are grateful to Pr. A. Osuna (Department of Parasitology, Faculty of Sciences, University of Granada, Spain) for helpful discussions. We thank Ms C. Jullien-Moutelon, C.G.M.C. Claude-Bernard University, for excellent technical assistance. The authors declare that the experiments comply with the current laws of the country in which the experiments were performed.

Author information

Authors and Affiliations

  1. Laboratory of Parasitology and Medical Mycology EA3741, Faculty of Pharmacy, Claude-Bernard University, 8, avenue Rockefeller, 69373, Lyon cedex 08, France

    M. Fraize, M. E. Sarciron, S. Azzouz, N. Issaadi & A. F. Petavy

  2. C.G.M.C., UMR CNRS 5534, Claude-Bernard University, Villeurbanne, France

    G. Bosquet

Authors
  1. M. Fraize
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. E. Sarciron
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Azzouz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Issaadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Bosquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. F. Petavy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. F. Petavy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fraize, M., Sarciron, M.E., Azzouz, S. et al. Immunogenicity of two Echinococcus granulosus antigens EgA31 and EgTrp in mice. Parasitol Res 96, 113–120 (2005). https://doi.org/10.1007/s00436-005-1322-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-005-1322-x

Keywords

Search

Navigation