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Schistosoma mansoni TOR is a tetraspanning orphan receptor on the parasite surface

Published online by Cambridge University Press:  13 March 2009

C. LOCHMATTER ,
J. A. SCHIFFERLI  and
P. J. MARTIN
C. LOCHMATTER*
Affiliation:
Department of Biomedicine, Immunonephrology, University Hospital Basel, Hebelstrasse 20, CH-4031 Basel, Switzerland
J. A. SCHIFFERLI
Affiliation:
Department of Biomedicine, Immunonephrology, University Hospital Basel, Hebelstrasse 20, CH-4031 Basel, Switzerland
P. J. MARTIN
Affiliation:
Department of Biomedicine, Immunonephrology, University Hospital Basel, Hebelstrasse 20, CH-4031 Basel, Switzerland
*
*Corresponding author. Tel: +41 61 2653891. Fax: +41 61 2652350. E-mail: c.lochmatter@unibas.ch
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Summary

A trispanning orphan receptor (TOR) has been described in Schistosoma haematobium and S. mansoni. Here we report the complete molecular organization of the S. mansoni TOR gene, also known as SmCRIT (complement C2 receptor inhibitor trispanning). The SmTOR gene consists of 4 exons and 3 introns as shown by cloning the single exons from S. mansoni genomic DNA and the corresponding cDNA from the larval stage (cercaria) and the adult worm. The SmTOR ORF consists of 1260 bp and is longer than previously reported, with a fourth trans-membrane domain (proposed new name: Tetraspanning Orphan Receptor) and with, however, an unchanged C2-binding domain on the extracellular domain 1 (ed1). This domain differs in S. japonicum. A protein at the approximate expected molecular weight (55 kDa) was detected in adult worm extracts with polyclonal and monoclonal antibodies, and was found to be expressed on the tegumental surface of cercariae.

Keywords

CRITTORSchistosomacomplement regulation
Type
Research Article
Information
Parasitology , Volume 136 , Issue 5 , April 2009 , pp. 487 - 498
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Bergquist, N. R., Leonardo, L. R. and Mitchell, G. F. (2005). Vaccine-linked chemotherapy: can schistosomiasis control benefit from an integrated approach? Trends in Parasitology 21, 112–117.CrossRefGoogle ScholarPubMed
Braschi, S., Borges, W. C. and Wilson, R. A. (2006 a). Proteomic analysis of the schistosome tegument and its surface membranes. Memorias Do Instituto Oswaldo Cruz 101, 205–212.CrossRefGoogle ScholarPubMed
Braschi, S., Curwen, R. S., Ashton, P. D., Verjovski-Almeida, S. and Wilson, A. (2006 b). The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6, 1471–1482.CrossRefGoogle ScholarPubMed
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular & Cellular Proteomics 5, 347–356. doi: 10.1074/mcp.M500287-MCP200CrossRefGoogle ScholarPubMed
Brouwers, J., Skelly, P. J., Van Golde, L. M. G. and Tielens, A. G. M. (1999). Studies on phospholipid turnover argue against sloughing of tegumental membranes in adult Schistosoma mansoni. Parasitology 119, 287–294.CrossRefGoogle ScholarPubMed
Claros, M. G. and Vonheijne, G. (1994). TopPred-II – an improved software for membrane-protein structure predictions. Computer Applications in the Biosciences 10, 685–686.Google ScholarPubMed
Correa-Oliveira, R., Caldas, I. R. and Gazzinelli, G. (2000). Natural versus drug-induced resistance in Schistosoma mansoni infection. Parasitology Today 16, 397–399.CrossRefGoogle ScholarPubMed
Correa-Oliveira, R., Pearce, E. J., Oliveira, G. C., Golgher, D. B., Katz, N., Bahia, L. G., Carvalho, O. S., Gazzinelli, G. and Sher, A. (1989). The human immune-response to defined immunogens of Schistosoma mansoni – elevated antibody levels to Paramyosin in stool-negative individuals from 2 endemic areas in Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 798–804.CrossRefGoogle ScholarPubMed
Dalton, J. P., Day, S. R., Drew, A. C. and Brindley, P. J. (1997). A method for the isolation of schistosome eggs and miracidia free of contaminating host tissues. Parasitology 115, 29–32.CrossRefGoogle ScholarPubMed
DeMarco, R., Mathieson, W., Dillon, G. P. and Wilson, R. A. (2007). Schistosome albumin is of host, not parasite, origin. International Journal for Parasitology 37, 1201–1208. doi: 10.1016/j.ijpara.2007.03.004CrossRefGoogle Scholar
Hamburger, J., Xu, Y. X., Ramzy, R. M., Jourdane, J. and Ruppel, A. (1998). Development and laboratory evaluation of a polymerase chain reaction for monitoring Schistosoma mansoni infestation of water. American Journal of Tropical Medicine and Hygiene 59, 468–473.CrossRefGoogle ScholarPubMed
Hansell, E., Braschi, S., Medzihradszky, K. F., Sajid, M., Debnath, M., Ingram, J., Lim, K. C. and McKerrow, J. H. (2008). Proteomic analysis of skin invasion by blood fluke larvae. PLoS Neglected Tropical Diseases 2, e262.CrossRefGoogle ScholarPubMed
Hooker, C. W. and Brindley, P. J. (1996). Cloning and characterisation of strain-specific transcripts encoding triosephosphate isomerase, a candidate vaccine antigen from Schistosoma japonicum. Molecular and Biochemical Parasitology 82, 265–269.CrossRefGoogle ScholarPubMed
Hui, K. M., Magnadottir, B., Schifferli, J. A. and Inal, J. M. (2006). CRIT peptide interacts with factor B and interferes with alternative pathway activation. Biochemical and Biophysical Research Communications 344, 308–314. doi: 10.1016/j.bbrc.2006.03.101CrossRefGoogle ScholarPubMed
Hui, K. M., Orriss, G. L., Schirmer, T., Magnadottir, B., Schifferli, J. A. and Inal, J. M. (2005). Expression of functional recombinant von Willebrand factor-A domain from human complement C2: a potential binding site for C4 and CRIT. The Biochemical Journal 389, 863–868. doi: 10.1042/bj20050183CrossRefGoogle Scholar
Inal, J. M. (1999). Schistosoma TOR (trispanning orphan receptor), a novel, antigenic surface receptor of the blood-dwelling, Schistosoma parasite. Biochimica et Biophysica Acta-Gene Structure and Expression 1445, 283–298.CrossRefGoogle ScholarPubMed
Inal, J. M. (2005). Complement C2 receptor inhibitor trispanning: from man to schistosome. Springer Seminars in Immunopathology 27, 320–331. doi: 10.1007/s00281-005-0009-9CrossRefGoogle Scholar
Inal, J. M., Hui, K. M., Miot, S., Lange, S., Ramirez, M. I., Schneider, B., Krueger, G. and Schifferli, J. A. (2005 b). Complement C2 receptor inhibitor trispanning: A novel human complement inhibitory receptor. Journal of Immunology 174, 356–366.CrossRefGoogle ScholarPubMed
Inal, J., Miot, S. and Schifferli, J. A. (2005 a). The complement inhibitor, CRIT, undergoes clathrin-dependent endocytosis. Experimental Cell Research 310, 54–65. doi: 10.1016/j.yexcr.2005.07.003CrossRefGoogle ScholarPubMed
Inal, J. M. and Schifferli, J. A. (2001). C4 beta chain peptide interferes with the formation of the classical pathway C2 convertase. Molecular Immunology 38, 97.Google Scholar
Inal, J. M. and Schifferli, J. A. (2002). Complement C2 receptor inhibitor trispanning and the beta-chain of C4 share a binding site for complement C2. Journal of Immunology 168, 5213–5221.CrossRefGoogle Scholar
Inal, J. M. and Sim, R. B. (2000). A Schistosoma protein, Sh-TOR, is a novel inhibitor of complement which binds human C2. FEBS Letters 470, 131–134.CrossRefGoogle ScholarPubMed
Jones, D. T. (1999). Protein secondary structure prediction based on position-specific scoring matrices. Journal of Molecular Biology 292, 195–202.CrossRefGoogle ScholarPubMed
Kemp, W. M., Brown, P. R., Merritt, S. C. and Miller, R. E. (1980). Tegument-associated antigen modulation by adult male Schistosoma mansoni. Journal of Immunology 124, 806–811.CrossRefGoogle ScholarPubMed
Kemp, W. M., Damian, R. T. and Greene, N. D. (1976). Immunocytochemical localisation of IgG on adult Schistosoma mansoni tegumental surfaces. Journal of Parasitology 62, 830–832.CrossRefGoogle ScholarPubMed
Kemp, W. M., Merritt, S. C. and Rosier, J. G. (1978). Schistosoma mansoni: Identification of immunoglobulins associated with tegument of adult parasites from mice. Experimental Parasitology 45, 81–87.CrossRefGoogle ScholarPubMed
Klabunde, J., Berger, J., Jensenius, J. C., Klinkert, M. Q., Zelck, U. E., Kremsner, P. G. and Kun, J. F. J. (2000). Schistosoma mansoni: Adhesion of mannan-binding lectin to surface glycoproteins of cercariae and adult worms. Experimental Parasitology 95, 231–239.CrossRefGoogle ScholarPubMed
Kool, J., Reubsaet, L., Wesseldijk, F., Maravilha, R. T., Pinkse, M. W., D'Santos, C. S., Van Hilten, J. J., Zijlstra, F. J. and Heck, A. J. (2007). Suction blister fluid as potential body fluid for biomarker proteins. Proteomics 7, 3638–3650.CrossRefGoogle ScholarPubMed
Kozak, M. (1984). Compilation and analysis of sequences upstream from the translation start site in eukaryotic mRNAs. Nucleic Acids Research 12, 857–872.CrossRefGoogle ScholarPubMed
Lessey, E., Li, N., Diaz, L. and Liu, Z. (2008). Complement and cutaneous autoimmune blistering diseases. Immunologic Research 41, 223–232.CrossRefGoogle ScholarPubMed
Linder, E. and Huldt, G. (1983). Antibody-independent binding and activation of complement by Schistosoma mansoni adult worms. Parasite Immunology 5, 183–194.Google ScholarPubMed
Liu, F., Lu, J., Hu, W., Wang, S. Y., Cui, S. J., Chi, M., Yan, Q., Wang, X. R., Song, H. D., Xu, X. N., Wang, J. J., Zhang, X. L., Zhang, X., Wang, Z. Q., Xue, C. L., Brindley, P. J., McManus, D. P., Yang, P. Y., Feng, Z., Chen, Z. and Han, Z. G. (2006). New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. Plos Pathogens 2, 268–281. doi: 10.1371/journal.ppat.0020029CrossRefGoogle ScholarPubMed
Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.CrossRefGoogle ScholarPubMed
Marikovsky, M., Parizade, M., Arnon, R. and Fishelson, Z. (1990). Complement regulation on the surface of cultured schistosomula and adult worms of Schistosoma mansoni. European Journal of Immunology 20, 221–227.CrossRefGoogle ScholarPubMed
McGuffin, L. J., Bryson, K. and Jones, D. T. (2000). The PSIPRED protein structure prediction server. Bioinformatics 16, 404–405.CrossRefGoogle ScholarPubMed
McManus, D. P. and Loukas, A. (2008). Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225–242.CrossRefGoogle ScholarPubMed
Minard, P., Dean, D. A., Jacobson, R. H., Vannier, W. E. and Murrell, K. D. (1978). Immunization of mice with Co-60 irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 76–86.CrossRefGoogle Scholar
Moll, S., Lange, S., Mihatsch, M., Dragic, Z., Schifferli, J. and Inal, J. (2006). CRIT is expressed on podocytes in normal human kidney and upregulated in membranous nephropathy. Kidney International 69, 1961–1968.CrossRefGoogle ScholarPubMed
Nakagawa, S. (2008). Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes. Nucleic Acids Research 36, 861–871.CrossRefGoogle ScholarPubMed
Pearce, E. J., Hall, B. F. and Sher, A. (1990). Host-specific evasion of the alternative complement pathway by schistosomes correlates with the presence of a phospholipase C-sensitive surface molecule resembling human decay accelerating factor. Journal of Immunology 144, 2751–2756.CrossRefGoogle ScholarPubMed
Ramalhopinto, F. J., Gazzinelli, G., Howells, R. E., Motasantos, T. A., Figueiredo, E. A. and Pellegrino, J. (1974). Schistosoma mansoni – defined system for stepwise transformation of cercaria to schistosomule in vitro. Experimental Parasitology 36, 360–372.CrossRefGoogle ScholarPubMed
Rasmussen, K. R. and Kemp, W. M. (1987). Schistosoma mansoni: interactions of adult parasites with the complement system. Parasite Immunology 9, 235–248.CrossRefGoogle ScholarPubMed
Roberts, S. M., MacGregor, A. N., Vojvodic, M., Wells, E., Crabtree, J. E. and Wilson, R. A. (1983). Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Molecular and Biochemical Parasitology 9, 105–127.CrossRefGoogle ScholarPubMed
Ross, A. G. P., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y. S., Williams, G. M. and McManus, D. P. (2002). Current concepts – schistosomiasis. New England Journal of Medicine 346, 1212–1220.CrossRefGoogle Scholar
Ruppel, A., McLaren, D. J., Diesfeld, H. J. and Rother, U. (1984). Schistosoma mansoni: escape from complement-mediated parasiticidal mechanisms following percutaneous primary infection. European Journal of Immunology 14, 702–708.CrossRefGoogle ScholarPubMed
Skelly, P. J. (2004). Immunoparasitology series: intravascular schistosomes and complement. Trends in Parasitology 20, 370–374. doi: 10.1016/j.pt.2004.05.007CrossRefGoogle Scholar
Skelly, P. J. and Wilson, R. A. (2006). Making sense of the schistosome surface. Advances in Parasitology 63, 185–284. doi: 10.1016/s0065-308x(06)63003-0CrossRefGoogle ScholarPubMed
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411–425.CrossRefGoogle ScholarPubMed
Stek, M., Minard, P., Dean, D. A. and Hall, J. E. (1981). Immunization of baboons with Schistosoma mansoni cercariae attenuated by gamma irradiation. Science 212, 1518–1520.CrossRefGoogle Scholar
Tendler, M. and Simpson, A. J. (2008). The biotechnology-value chain: development of Sm14 as a schistosomiasis vaccine. Acta Tropica 108, 263–266.CrossRefGoogle ScholarPubMed
Timar, K. K., Dallos, A., Kiss, M., Husz, S., Bos, J. D. and Asghar, S. S. (2007). Expression of terminal complement components by human keratinocytes. Molecular Immunology 44, 2578–2586.CrossRefGoogle ScholarPubMed
Tran, M. H., Pearson, M. S., Jeffrey, M. B., 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 Balkom, B. W. M., Van Gestel, R. A., Brouwers, J., Krijgsveld, J., Tielens, A. G. M., Heck, A. J. R. and Van Hellemond, J. J. (2005). Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. Journal of Proteome Research 4, 958–966. doi: 10.1021/pr050036wCrossRefGoogle ScholarPubMed