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Cloning and characterization of an orphan seven transmembrane receptor from Schistosoma mansoni

Published online by Cambridge University Press:  23 August 2007

M. S. PEARSON ,
D. P. McMANUS ,
D. J. SMYTH ,
M. K. JONES ,
A. M. SYKES  and
A. LOUKAS
M. S. PEARSON*
Affiliation:
Division of Infectious Diseases and Immunology, Queensland Institute of Medical Research and Australian Centre for International and Tropical Health and Nutrition, The University of Queensland, Brisbane, Queensland, Australia
D. P. McMANUS
Affiliation:
Division of Infectious Diseases and Immunology, Queensland Institute of Medical Research and Australian Centre for International and Tropical Health and Nutrition, The University of Queensland, Brisbane, Queensland, Australia
D. J. SMYTH
Affiliation:
Division of Infectious Diseases and Immunology, Queensland Institute of Medical Research and Australian Centre for International and Tropical Health and Nutrition, The University of Queensland, Brisbane, Queensland, Australia
M. K. JONES
Affiliation:
Division of Infectious Diseases and Immunology, Queensland Institute of Medical Research and Australian Centre for International and Tropical Health and Nutrition, The University of Queensland, Brisbane, Queensland, Australia
A. M. SYKES
Affiliation:
Division of Infectious Diseases and Immunology, Queensland Institute of Medical Research and Australian Centre for International and Tropical Health and Nutrition, The University of Queensland, Brisbane, Queensland, Australia
A. LOUKAS*
Affiliation:
Division of Infectious Diseases and Immunology, Queensland Institute of Medical Research and Australian Centre for International and Tropical Health and Nutrition, The University of Queensland, Brisbane, Queensland, Australia
*
*Corresponding authors: Tel: 61 7 3845 3702. Fax: 61 7 3845 3507. E-mail: [email protected] or [email protected]
*Corresponding authors: Tel: 61 7 3845 3702. Fax: 61 7 3845 3507. E-mail: [email protected] or [email protected]
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Summary

A partial cDNA sequence was obtained from the human blood fluke, Schistosoma mansoni using a signal sequence trap approach. The full-length cDNA was cloned and termed Sm-7TM. The corresponding open reading frame had 7 membrane spanning domains and shared identity with a small, novel group of seven transmembrane (7TM) receptors from vertebrates and invertebrates, including the human ee3 receptor – a heptahelical protein implicated in neuronal signalling. Phylogenetic analysis of this novel family showed that the Sm-7TM ORF formed a clade with exclusively invertebrate sequences. Based on topology modelling with ee3, Sm-7TM was predicted to possess an intracellular C-terminal tail, which was expressed as a soluble thioredoxin fusion protein (Sm-7TMC) in Escherichia coli and purified using metal ion-affinity chromatography. A polyclonal antiserum against this domain was used to detect Sm-7TM in detergent-soluble parasite extracts and to immunolocalize the receptor to the tegument of adult S. mansoni.

Keywords

Schistosoma mansoniseven transmembrane receptortegument
Type
Research Article
Information
Parasitology , Volume 134 , Issue 14 , December 2007 , pp. 2001 - 2008
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Basch, P. F. (1981). Cultivation of Schsitosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. Journal of Parasitology 67, 179–185.CrossRefGoogle Scholar
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular and Cellular Proteomics 5, 347–356.CrossRefGoogle ScholarPubMed
Braschi, S., Curwen, R. S., Ashton, P. D., Verjovski-Almeida, S. and Wilson, A. (2006). The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6, 1471–1482.CrossRefGoogle ScholarPubMed
Capron, A., Riveau, G., Capron, M. and Trottein, F. (2005). Schistosomes: the road from host-parasite interactions to vaccines in clinical trials. Trends in Parasitology 21, 143–149.CrossRefGoogle ScholarPubMed
Da'dara, A. A., Skelly, P. J., Wang, M. M. and Harn, D. A. (2001). Immunization with plasmid DNA encoding the integral membrane protein, Sm23, elicits a protective immune response against schistosome infection in mice. Vaccine 20, 359–369.CrossRefGoogle ScholarPubMed
Hamdan, F. F., Abramovitz, M., Mousa, A., Xie, J., Durocher, Y. and Ribeiro, P. (2002). A novel Schistosoma mansoni G protein-coupled receptor is responsive to histamine. Molecular and Biochemical Parasitology 119, 75–86.CrossRefGoogle ScholarPubMed
Hoffmann, K. F., Davis, E. M., Fischer, E. R. and Wynn, T. A. (2001). The guanine protein coupled receptor rhodopsin is developmentally regulated in the free-living stages of Schistosoma mansoni. Molecular and Biochemical Parasitology 112, 113–123.CrossRefGoogle ScholarPubMed
Hu, W., Yan, Q., Shen, D. K., Liu, F., Zhu, Z. D., Song, H. D., Xu, X. R., Wang, Z. J., Rong, Y. P., Zeng, L. C., Wu, J., Zhang, X., Wang, J. J., Xu, X. N., Wang, S. Y., Fu, G., Zhang, X. L., Wang, Z. Q., Brindley, P. J., McManus, D. P., Xue, C. L., Feng, Z., Chen, Z. and Han, Z. G. (2003). Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139–147.CrossRefGoogle ScholarPubMed
Karchin, R., Karplus, K. and Haussler, D. (2002). Classifying G-protein coupled receptors with support vector machines. Bioinformatics 18, 147–159.CrossRefGoogle ScholarPubMed
King, C. H., Dickman, K. and Tisch, D. J. (2005). Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561–1569.CrossRefGoogle ScholarPubMed
Lefkowitz, R. J. (2004). Historical review: a brief history and personal retrospective of seven-transmembrane receptors. Trends in Pharmacological Sciences 25, 413–422.CrossRefGoogle ScholarPubMed
Li, Y., Auliff, A., Jones, M. K., Yi, X. and McManus, D. P. (2000). Immunogenicity and immunolocalization of the 22·6 kDa antigen of Schistosoma japonicum. Parasite Immunology 22, 415–424.CrossRefGoogle ScholarPubMed
Loukas, A., Tran, M. and Pearson, M. S. (2007). Schistosome membrane proteins as vaccines. International Journal for Parasitology 37, 257–263.CrossRefGoogle ScholarPubMed
Maurer, M. H., Grunewald, S., Gassler, N., Rossner, M., Propst, F., Wurz, R., Weber, D., Kuner, T., Kuschinsky, W. and Schneider, A. (2004). Cloning of a novel neuronally expressed orphan G-protein-coupled receptor which is up-regulated by erythropoietin, interacts with microtubule-associated protein 1b and colocalizes with the 5-hydroxytryptamine 2a receptor. Journal of Neurochemistry 91, 1007–1017.CrossRefGoogle Scholar
Mombaerts, P. (1999). Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286, 707–711.CrossRefGoogle ScholarPubMed
Pearson, M. S., McManus, D. P., Smyth, D. J., Lewis, F. A. and Loukas, A. (2005). In vitro and in silico analysis of signal peptides from the human blood fluke, Schistosoma mansoni. FEMS Immunology and Medical Microbiology 45, 201–211.CrossRefGoogle ScholarPubMed
Pierce, K. L., Premont, R. T. and Lefkowitz, R. J. (2002). Seven-transmembrane receptors. Nature Reviews. Molecular Cell Biology 3, 639–650.CrossRefGoogle ScholarPubMed
Ross, A. G., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. (2002). Schistosomiasis. New England Journal of Medicine 346, 1212–1220.CrossRefGoogle ScholarPubMed
Smithers, S. R., Hackett, F., Ali, P. O. and Simpson, A. J. (1989). Protective immunization of mice against Schistosoma mansoni with purified adult worm surface membranes. Parasite Immunology 11, 301–318.CrossRefGoogle ScholarPubMed
Smyth, D., McManus, D. P., Smout, M. J., Laha, T., Zhang, W. and Loukas, A. (2003). Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infection and Immunity 71, 2548–2554.CrossRefGoogle ScholarPubMed
Spiess, M. (1995). Heads or tails – what determines the orientation of proteins in the membranes? FEBS Letters 369, 76–79.CrossRefGoogle ScholarPubMed
Suri, P. K., Goldberg, M., Madikizela, M., Petzke, M. M., Bungiro, R. D. Jr., Davies, S. J., Chakraborty, B., Nguyen, K. B., McCray, J. W. Jr. and Knopf, P. M. (1997). Evaluation of recombinant protein r140, a polypeptide segment of tegumental glycoprotein Sm25, as a defined antigen vaccine against Schistosoma mansoni. Parasite Immunology 19, 515–529.CrossRefGoogle ScholarPubMed
Tendler, M., Brito, C. A., Vilar, M. M., Serra-Freire, N., Diogo, C. M., Almeida, M. S., Delbem, A. C., Da Silva, J. F., Savino, W., Garratt, R. C., Katz, N. and Simpson, A. S. (1996). A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proceedings of the National Academy of Sciences, USA 93, 269–273.CrossRefGoogle ScholarPubMed
Todd, C. W. and Colley, D. G. (2002). Practical and ethical issues in the development of a vaccine against schistosomiasis mansoni. American Journal of Tropical Medicine and Hygiene 66, 348–358.CrossRefGoogle ScholarPubMed
Tran, M. H., Pearson, M. S., Bethony, J. M., Smyth, D. J., Jones, M. K., Duke, M., Don, T. A., McManus, D. P., Correa-Oliveira, R. and Loukas, A. (2006). Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Medicine 12, 835–840.CrossRefGoogle ScholarPubMed
van der Werf, M. J., de Vlas, S. J., Brooker, S., Looman, C. W., Nagelkerke, N. J., Habbema, J. D. and Engels, D. (2003). Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86, 125–139.CrossRefGoogle ScholarPubMed
Verjovski-Almeida, S., DeMarco, R., Martins, E. A., Guimaraes, P. E., Ojopi, E. P., Paquola, A. C., Piazza, J. P., Nishiyama, M. Y. Jr., Kitajima, J. P., Adamson, R. E., Ashton, P. D., Bonaldo, M. F., Coulson, P. S., Dillon, G. P., Farias, L. P., Gregorio, S. P., Ho, P. L., Leite, R. A., Malaquias, L. C., Marques, R. C., Miyasato, P. A., Nascimento, A. L., Ohlweiler, F. P., Reis, E. M., Ribeiro, M. A., Sa, R. G., Stukart, G. C., Soares, M. B., Gargioni, C., Kawano, T., Rodrigues, V., Madeira, A. M., Wilson, R. A., Menck, C. F., Setubal, J. C., Leite, L. C. and Dias-Neto, E. (2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148–157.CrossRefGoogle ScholarPubMed