Abstract
Two clones from an activated Taenia saginata oncosphere cDNA library, Ts45W and Ts45S, were isolated and sequenced. Both of these genes belong to the Taenia ovis 45W gene family. The Ts45W and Ts45S cDNAs are 997- and 1,004-bp-long, each corresponding to 255 amino acids and with theoretical molecular masses of 27.8 and 27.7 kDa, respectively. Southern blot profiles obtained with Ts45W cDNA as a probe suggest that these two genes are members of a multigene family with tandem organization. The full genomic sequence was determined for the Ts45W gene and a new family member, the Ts45W/2 gene. The genomic sequences of the T. saginata Ts45W and Ts45W/2 genes were at least 2.2 kb in length with four exons separated by three introns. Exons 1 and 4 coded for hydrophobic domains, while, importantly, exons 2 and 3 coded for fibronectin homologous domains. These domains are presumably responsible for the demonstrated cell adhesion and, perhaps, the protective nature of this family of molecules and the acronym TAF (Taenia adhesion family) is proposed for this group of genes. We hypothesize that these TAF proteins and another T. saginata-protective antigen, HP6, have evolved the dual functions of facilitating tissue invasion and stimulating protective immunity to first ensure primary infection and subsequently to establish a concomitant protective immunity to protect the host from death or debilitation through superinfection by subsequent infections and thus help ensure parasite survival.
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References
Altschul SF, Madden TL, Schffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Benitez L, Garate T, Harrison LJ, Kirkham P, Brookes SM, Parkhouse RM (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
Benitez L, Harrison LJ, Parkhouse RM, Gonzalez LM, Gottstein B, Garate T (1998) Sequence and immunogenicity of the Taenia saginata homologue of the major surface antigen of Echinococcus spp. Parasitol Res 84:426–431
Bonay P, Gonzalez LM, Benitez L, Foster M, Harrison LJ, Parkhouse RM, Garate T (2002) Genomic and functional characterisation of a secreted antigen of Taenia saginata oncospheres. Mol Biochem Parasitol 121:269–273
Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Bucher P, Bairoch A (1994) A generalized profile syntax for biomolecular sequence motifs and its function in automatic sequence interpretation. Proc Int Conf Intell Syst Mol Biol 2:53–61
Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94
Burge WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448
Chow C, Gauci CG, Cowman AF, Lightowlers MW (2001) A gene family expressing a host-protective antigen of Echinococcus granulosus. Mol Biochem Parasitol 118:83–88.16
Cserzo M, Wallin E, Simon I, von Heijne G, Elofsson A (1997) Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10:673–676
Drew DR, Lightowlers M, Strugnell RA (2000) Humoral immune responses to DNA vaccines expressing secreted, membrane bound and non-secreted forms of the Taenia ovis 45W antigen. Vaccine 18:2522–2532
Gauci CG, Lightowlers MW (2001) Alternative splicing and sequence diversity of transcripts from the oncosphere stage of Taenia solium with homology to the 45W antigen of Taenia ovis. Mol Biochem Parasitol 112:173–181
Gauci C, Lightowlers MW (2003) Molecular cloning of genes encoding oncosphere proteins reveals conservation of modular protein structure in cestode antigens. Mol Biochem Parasitol 127:193–198
Gauci CG, Flisser A, Lightowlers MW (1998) A Taenia solium oncosphere protein homologous to host-protective Taenia ovis and Taenia saginata 18 kDa antigens. Int J Parasitol 28:757–760
Gauci C, Merli M, Muller V, Chow C, Yagi K, Mackenstedt U, Lightowlers MW (2002) Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infect Immun 70:3969–3972
Green ED, Olson MV (1990) Systematic screening of yeast artificial-chromosome libraries by use of the polymerase chain reaction. Proc Natl Acad Sci USA 87:1213–1217
Harrison LJS, Parkhouse RME (1986) Passive protection against Taenia saginata infection in cattle by a mouse monoclonal antibody reactive with the surface of the invasive oncospheres. Parasite Immunol 8:319–332
Harrison LJS, Parkhouse RME (1994) Antigens of parasitic helminths in protection and pathology. In: Chowdhury, N (ed) Helminthology. Narosa Publishing House and Springer Verlag Ltd, pp 258–271
Harrison GB, Heath DD, Dempster RP, Gauci C, Newton SE, Cameron WG, Robinson CM, Lawrence SB, Lightowlers MW, Rickard MD (1996) Identification and cDNA cloning of two novel low molecular weight host-protective antigens from Taenia ovis oncospheres. Int J Parasitol 26:195–204
Harrison LJ, Garate T, Bryce DM, Gonzalez LM, Foster-Cuevas M, Wamae LW, Onyango-Abuje JA, Parkhouse RM (2005) Ag-ELISA and PCR for monitoring the vaccination of cattle against Taenia saginata cysticercosis using an oncospheral adhesion protein (HP6) with surface and secreted localization. Trop Anim Health Prod 37:103–120
Johnson KS, Harrison GB, Lightowlers MW, O’Hoy KL, Cougle WG, Dempster RP, Lawrence SB, Vinton JG, Heath DD, Rickard MD (1989) Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature 338:585–587
Kozak M (1984) Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 12:857–872
Lightowlers MW, Gauci CG (2001) Vaccines against cysticercosis and hydatidosis. Vet Parasitol 101:337–352
Lightowlers MW, Lawrence SB, Gauci CG, Young J, Ralston MJ, Maas D, Health DD (1996a) Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunol 18:457–462
Lightowlers MW, Rolfe R, Gauci CG (1996b) Taenia saginata: vaccination against cysticercosis in cattle with recombinant oncosphere antigens. Exp Parasitol 84:330–338
Lightowlers MW, Colebrook AL, Gauci CG, Gauci SM, Kyngdon CT, Monkhouse JL, Vallejo Rodriguez C, Read AJ, Rolfe RA, Sato C (2003a) Vaccination against cestode parasites: anti-helminth vaccines that work and why. Vet Parasitol 115:83–123
Lightowlers MW, Gauci CG, Chow C, Drew DR, Gauci SM, Heath DD, Jackson DC, Dadley-Moore DL, Read AJ (2003b) Molecular and genetic characterisation of the host-protective oncosphere antigens of taeniid cestode parasites. Int J Parasitol 33:1207–1217
McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16:404–405
Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int J Neural Syst 8:581–599
Parkhouse RME, Garate T, Benitez L, Kirkham P, Brookes SM, Wright SH, Harrison LJS (1996) Approaches towards a vaccines for human porcine and bovine cysticercosis. In: Garcia HH, Martinez-M SM (eds) Taenia solium. Taeniasis/Cysticercosis. Editorial Universo, Lima, Peru, pp 121–131
Pearce EJ, Sher A (1989) Three major surface antigens of Schistosoma mansoni are linked to the membrane by glycosylphosphatidylinositol. J Immunol 142:979–984
Periman D, Halvorsan HO (1983) A putative signal peptidase recognition site and sequences in eukaryotic and prokaryotic signal peptides. J Mol Biol 167:391–409
Plancarte A, Flisser A, Gauci CG, Lightowlers MW (1999) Vaccination against Taenia solium cysticercosis in pigs using native and recombinant oncosphere antigens. Int J Parasitol 29:643–647
Rosas G, Fragoso G, Garate T, Hernandez B, Ferrero P, Foster-Cuevas M, Parkouse RME, Harrison L, Lopez-Briones S, Gonzalez LM, Sciutto E (2002) Protective immunity against Taenia crassiceps murine cysticercosis induced by DNA vaccination with a Taenia saginata tegument antigen. Microbes Infect 4:1417–1426
Sachs A, Wahle E (1993) Poly(A) tail metabolism and function in eucaryotes. J Biol Chem 268:22955–22958
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor, New York
Schofield L, Hackett F (1993) Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 177:145–153
Schofield L, Gerold P, Schwarz RT, Tachado S (1994) Signal transduction in host cells mediated by glycosylphosphatidylinositols of the parasitic protozoa, or why do the parasitic protozoa have so many GPI molecules? Braz J Med Biol Res 27:249–254
Senapathy P, Shapiro MB, Harris NL (1990) Splice junctions, branch point sites, and exons: sequence statistics, identification, and applications to genome project. Methods Enzymol 183:252–278
Short JM, Fernandez JM, Sorge JA, Huse WD (1988) Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. Nucleic Acids Res 16:7583–7600
Simpson AJ, Sher A, McCutchan TF (1982) The genome of Schistosoma mansoni: isolation of DNA, its size, bases and repetitive sequences. Mol Biochem Parasitol 6:125–137
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517
Solovyev VV, Salamov AA, Lawrence CB (1995) Identification of human gene structure using linear discriminant functions and dynamic programming. Proc Int Conf Intell Syst Mol Biol 3:367–375
Tachado SD, Mazhari-Tabrizi R, Schofield L (1999) Specificity in signal transduction among glycosylphosphatidylinositols of Plasmodium falciparum, Trypanosoma brucei, Trypanosoma cruzi and Leishmania spp. Parasite Immunol 21:609–617
Waterkeyn JG, Lightowlers MW, Coppel R, Cowman AF (1995) Characterization of the gene family encoding a host-protective antigen of the tapeworm Taenia ovis. Mol Biochem Parasitol 73:123–131
Xu X, Caulfield JP (1992) Characterization of human low density lipoprotein binding proteins on the surface of schistosomula of Schistosoma mansoni. Eur J Cell Biol 57:229–235
Acknowledgements
This work was supported by grants from EU-INCO-DC (grant CT95-0002 #1274/05), FIS, ISCIII-Programa Intramural (00-47, 00-625, MPY 1114/03, and MPY 1274/05), RICET. LM Gonzalez was sponsored by fellowships from ISCIII and RICET-FIS. The experiments described in this paper comply with the current laws of the country in which they were performed.
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Gonzalez, L.M., Bonay, P., Benitez, L. et al. Molecular and functional characterization of a Taenia adhesion gene family (TAF) encoding potential protective antigens of Taenia saginata oncospheres. Parasitol Res 100, 519–528 (2007). https://doi.org/10.1007/s00436-006-0297-6
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DOI: https://doi.org/10.1007/s00436-006-0297-6