Skip to main content

Advertisement

SpringerLink
Log in

Cloning and characterization of Taenia saginata paramyosin cDNA

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

Abstract

A λZAP-express cDNA library of Taenia saginata metacestodes was constructed. Antibody screening yielded a clone with an insert of 3,408 bp, an open reading frame of 2,589 bp, a deduced sequence of 863 amino acid and a molecular mass of 98.89 kDa. Alignments of the predicted amino acid sequence showed identity with paramyosins from several species: 98.8% with Taenia solium, 96.3% with Echinococcus.granulosus and about 70% with Schistosoma spp. The insert was expressed and purified. A collagen binding assay was performed which showed that T. saginata GST-paramyosin retained this property in a dose-dependent manner. Problems were encountered due to high backgrounds in serological assays in the homologous T. saginata system. However, the recombinant paramyosin was recognized by antibodies present in 31.6% of sera from T. solium seropositive cysticercosis patients and 100% of the sera from acute cysticercosis patients. The immunodominant epitope was the carboxyl-terminal fragment of the molecule.

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

  • Andrade MA, Brown NP, Leroy C, Hoersch S, De Daruvar A, Reich C, Franchini A, Tamames J, Valencia A, Ouzounis C, Sander C (1999) Automated genome sequence analysis and annotation. Bioinformatics 15:391-412

    Article  CAS  PubMed  Google Scholar 

  • Benitez L, Garate T, Harrison LJS, Kirkham P, Brookes SM, Parkhouse RME (1996) Cloning and sequencing of the gene encoding the principal 18-kDa secreted antigen of activated oncospheres of Taenia saginata. Mol Biochem Parasitol 78:265-268

    Google Scholar 

  • Chung JY, Bahk YY, Huh S, Kang SY, Kong,Y Cho SY (1999) A recombinant 10 kDa protein of Taenia solium metacestodes specific to active neurocysticercosis. J Infect Dis 180:1307–1315

    Article  CAS  PubMed  Google Scholar 

  • Cohen C, Szent-Györgyi AG, Kendrick-Jones J (1971) Paramyosin and the filaments of molluscan "catch" muscles. I. Paramyosin: structure and assembly. J Mol Biol 56:223–237

    CAS  PubMed  Google Scholar 

  • Devereux JR, Haeberli PL, Smithies O (1984) A comprehensive set of sequence analysis programmes for the VAX. Nucleic Acid Res 12:387–395

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Flisser A, Woodhouse E, Larralde C (1980) Human cysticercosis antigens, antibodies and non-responders. Clin Exp Immunol 39:27–37

    CAS  PubMed  Google Scholar 

  • Flisser A, Espinoza B, Tovar A, Plancarte A, Correa D (1986) Host-parasite relationship in cysticercosis: immunologic study in different compartments of the host. Vet Parasitol 20:95–102

    Google Scholar 

  • Gross Z, Ram D, Markovics A (1990) Schistosoma mansoni: stage-specific expression of muscle-specific genes. Exp Parasitol 70:62–71

    Google Scholar 

  • Harrison LJS, Joshua GWP, Wright SH, Parkhouse RME (1989) Specific detection of circulating surface/secreted glycoproteins of viable cysticerci in Taenia saginata cysticercosis. Parasite Immunol 11:351–370

    Google Scholar 

  • Hirsch C, Carvalho-Queiroz C, Franco G, Pena S, Simpson A, Goes AM (1997) Evidentiation of paramyosin (Sm97) as a modulating antigen on granulomatous hypersensitivity to Schistosoma mansoni eggs. Mem Inst Oswaldo Cruz 92:663–667

    CAS  PubMed  Google Scholar 

  • James SL, Pearce EJ, Sher A (1985) Induction of protective immunity against Schistosoma mansoni by a non living vaccine. I. Partial characterization of antigens recognized by antibodies from mice immunized with soluble schistosome extracts. J Immunol 134:3432–3434

    CAS  PubMed  Google Scholar 

  • Jameson BA, Wolf H (1988) The antigenic index: a novel algorithm for predicting antigenic determinants. Comput Appl Biosci 4:181-186

    CAS  PubMed  Google Scholar 

  • Kagawa H, Gengyo K, McLachlan AD, Brener S, Karn J (1989) The paramyosin gene (unc-15) of Caenorhabditis elegans: molecular cloning, nucleotide sequence and models for thick filament assembly. J Mol Biol 207:311–333

    CAS  PubMed  Google Scholar 

  • Kalinna BH, McManus DP (1997) A vaccine against the Asian schistosome, Schistosoma japonicum: an update on paramyosine as a target of protective immunity. Int J Parasitol 27:1213–1219

    CAS  PubMed  Google Scholar 

  • Laclette JP, Merchant MT, Willms K (1987) Histological and ultrastructural localization of antigen B in the metacestode of Taenia solium. J Parasitol 73: 121–129

    Google Scholar 

  • Laclette JP, Landa A, Arcos L, Willms K, Davis AE, Shoemaker CB (1991) Paramyosin is the Schistosoma mansoni (Trematoda) homologue of antigen B from Taenia solium (Cestoda). Mol Biochem Parasitol 44:287–296

    CAS  PubMed  Google Scholar 

  • Laclette JP, Shoemaker CB, Richter D, Arcos L, Pante N, Cohen C, Bing D, Nicholson-Weller A (1992) Paramyosin inhibits complement C1. J Immunol 148:124–128

    CAS  PubMed  Google Scholar 

  • Landa A, Laclette JP, Nicholson-Weller A, Shoemaker CB (1993) cDNA cloning and recombinant expression of collagen-binding and complement inhibitor activity of Taenia solium paramyosin (Ag B). Mol Biochem Parasitol 60:343–348

    CAS  PubMed  Google Scholar 

  • Langy S, Plinchart C, Luquiand P, Williams SA, Nicolas L (1998) The immunodominant Brugia malayi paramyosin as a marker of current infection with Wuchereria bancrofti adult worms. Infect Immun 86:2854–2858

    Google Scholar 

  • Larralde C, Laclette JP, Owen CS, Madrazo I, Sandoval M, Bojalil R, Sciutto E, Contreras L, Arzate J, Diaz ML (1986) Reliable serology of Taenia solium cysticercosis with antigens from cyst vesicular fluid: ELISA and hemaglutination tests. Am J Trop Med Hyg 35:965–973

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Limberger RJ, McReynolds LA (1990) Filarial paramyosin—cDNA sequences from Dirofilaria imitis and Onchocerca volvulus. Mol Biochem Parasitol 38:271-280

    CAS  PubMed  Google Scholar 

  • Matsumoto Y, Perry G, Levine RJC, Blanton R, Mahmoud AAF, Aikawa M (1988) Paramyosin and actin in schistosomal teguments. Nature 333:76–78

    CAS  PubMed  Google Scholar 

  • Mühlschlegel F, Sygulla L, Frosch P, Massetti P, Frosch M (1993) Paramyosine of Echinococcus granulosus: cDNA sequence and characterization of a tegumental antigen. Parasitol Res 79:660–666

    CAS  PubMed  Google Scholar 

  • Nara T, Tanabe K, Mahakunkijcharoen Y et al. (1997) The B cell epitope of paramyosine recognized by a protective monoclonal IgE antibody to Schistosoma japonicum. Vaccine 15:79–84

    Article  CAS  PubMed  Google Scholar 

  • Nielsen H, Engelbrednt J, Brunak S, Von Hefine G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1-6

    CAS  Google Scholar 

  • Pearce EJ, James SL, Dalton J, Barrall A, Ramos C, Strand M, Sher A (1986) Immunochemical characterization and purification of Sm-97, a Schistosoma mansoni antigen monospecifically recognized by antibodies from mice protectively immunized with a nonliving vaccine. J Immunol 137:3593–3600

    CAS  PubMed  Google Scholar 

  • Ramírez BL, Kurtis,JD, Wiest PM, Arias P, Aligui F, Acosta L, Peters P, Olds GR (1996) Paramyosin: a candidate vaccine antigen against Schistosoma japonicum. Parasite Immunol 18: 49–52

    CAS  PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc.Natl Acad Sci U S A 74:5463–5467

    CAS  PubMed  Google Scholar 

  • Steel C, Limberger R, McReynolds L, Ottesen E, Nutman T (1990) B cell responses to Paramyosin. J Immunol 145:3917–3923

    CAS  PubMed  Google Scholar 

  • Stevenson P (1983) Observations on the hatching and activation of fresh Taenia saginata eggs. Ann Trop Med Parasitol 77:399–404

    CAS  PubMed  Google Scholar 

  • Vazquez-Talavera J, Solis CF, Terrazas LI, Laclette JP (2001a) Characterization and protective potential of the immune response to Taenia solium paramyosin in a murine model of cysticercosis. Infect Immun 69:5412-5416

    Article  PubMed  Google Scholar 

  • Vazquez-Talavera J, Solis CF, Medina-Escutia E, Lopez ZM, Proano J, Correa D, Laclette JP (2001b) Human T and B cell epitope mapping of Taenia solium paramyosin. Parasite Immunol 23:575-579

    Article  PubMed  Google Scholar 

  • Vinós J, Domingo A, Marco R, Cervera M (1991) Identification and characterization of Drosophila melanogaster paramyosin. J Mol Biol 220:687–700

    PubMed  Google Scholar 

Download references

Acknowledgements

This investigation received financial support from INCO-DC project CT95-0002 of the European Union. Eva Moyano, Laura Benitez and Luis Miguel González were supported by a grant from ISCIII. Elizabeth Ferrer was supported by a grant from AECI and ISCIII. The authors would like to thank Maria Lares, Glenda Rojas, Yenny Alviarez for their collaboration in the collection of serum samples, Mercedes Rodríguez for technical assistance in immunodiagnosis assays and Drs. J.A. Onyango-Abuje and L.W. Wamae, and staff at the National Veterinary Research Centre, P.O.B. 32, Muguga, Kenya for collecting the T. saginata eggs.

Author information

Authors and Affiliations

  1. Instituto de Salud Carlos III, Centro Nacional de Microbiología, 28220 Majadahonda, Madrid, Spain

    Elizabeth Ferrer, Eva Moyano, Laura Benitez, Luis Miguel González & Teresa Gárate

  2. Department of Tropical Animal Health, Sir Alexander Robertson Centre for Tropical Veterinary Medicine, Easter Bush Veterinary Centre, University of Edinburgh, EH25 9RG, Roslin, Midlothian, Scotland

    Denise Bryce & Leslie J. S. Harrison

  3. Institute for Animal Health, Pirbright Laboratories, Woking, Surrey, England

    Mildred Foster-Cuevas

  4. Departamento de Parasitología, Universidad de Carabobo, Valencia, Venezuela

    Iris Dávila

  5. Centro de Investigaciones Biomédicas (BIOMED) Universidad de Carabobo, Maracay, Venezuela

    Maria Milagros Cortéz

  6. Instituto Gulbenkian de Ciéncia, Rua Quinta Grande 6, 2780–156, Oeiras, Portugal

    R. Michael E. Parkhouse

  7. Departamento de Microbiología-III, Facultad de Biología, Universidad Complutense (UCM), Madrid, Spain

    Laura Benitez

  8. Sir William Dunn School of Pathology, University of Oxford, OX1 3RE, Oxford, England

    Mildred Foster-Cuevas

Authors
  1. Elizabeth Ferrer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva Moyano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Benitez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luis Miguel González
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Denise Bryce
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mildred Foster-Cuevas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Iris Dávila
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Milagros Cortéz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Leslie J. S. Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. R. Michael E. Parkhouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Teresa Gárate
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leslie J. S. Harrison.

Additional information

Nucleotide sequence data reported in this paper has been submitted to the GenBank, EMBL and DDBJ databases under the accession number AJ439882

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrer, E., Moyano, E., Benitez, L. et al. Cloning and characterization of Taenia saginata paramyosin cDNA. Parasitol Res 91, 60–67 (2003). https://doi.org/10.1007/s00436-003-0895-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-003-0895-5

Keywords

Search

Navigation