Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T00:54:41.943Z Has data issue: false hasContentIssue false
  • English
  • Français

Der-p2 (Dermatophagoides pteronyssinus) allergen-like protein from the hard tick Ixodes ricinus – a novel member of ML (MD-2-related lipid-recognition) domain protein family

Published online by Cambridge University Press:  14 April 2010

J. HORÁČKOVÁ ,
N. RUDENKO ,
M. GOLOVCHENKO  and
L. GRUBHOFFER
J. HORÁČKOVÁ*
Affiliation:
Faculty of Science, University of South Bohemia and Biology Centre AS CR, Institute of Parasitology, Branišovská 31, 370 05 České Budějovice, Czech Republic
N. RUDENKO
Affiliation:
Faculty of Science, University of South Bohemia and Biology Centre AS CR, Institute of Parasitology, Branišovská 31, 370 05 České Budějovice, Czech Republic
M. GOLOVCHENKO
Affiliation:
Faculty of Science, University of South Bohemia and Biology Centre AS CR, Institute of Parasitology, Branišovská 31, 370 05 České Budějovice, Czech Republic
L. GRUBHOFFER
Affiliation:
Faculty of Science, University of South Bohemia and Biology Centre AS CR, Institute of Parasitology, Branišovská 31, 370 05 České Budějovice, Czech Republic
*
*Corresponding author: Tel: +42 0387775447. Fax: +42 0385310388. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

Objective. Expression of the gene encoding Der-p2 allergen-like protein in the castor bean tick Ixodes ricinus is induced by blood intake. Tick Der-p2 allergen-like protein belongs to a diverse family of ML proteins that includes major allergens of house dust mites, human MD-2 or similar proteins from Drosophila melanogaster. In ticks, genes encoding proteins belonging to the ML protein family were identified, but their protein products have not been characterized yet. Methods. A gene encoding tick Der-p2 allergen-like protein was amplified from cDNA of engorged I. ricinus female using the gene-specific primers designed on a basis of partial sequences of related allergen-like genes. The tissue and state specific patterns of expression of the gene were analysed. The IgE binding activity of the produced recombinant protein was studied by use of ELISA. Results. Analysis of the expression pattern showed that the gene encoding the tick Der-p2 allergen-like protein is strongly induced by the bloodmeal in gut and haemolymph throughout all tick developmental stages. Der-p2 allergen-like protein possesses a putative lipid-binding site, according to the comparisons with the related proteins. The ability of tick Der-p2 allergen-like protein to bind immunoglobulin E (IgE) was revealed. Discussion. The presence of a putative lipid-binding domain in Der-p2 allergen-like protein and its ability to interact with IgE might indicate the involvement of the protein in the tick's immune response.

Keywords

Der-p2 allergen-like proteinIxodes ricinustickML protein familyIgE-binding activity
Type
Research Article
Information
Parasitology , Volume 137 , Issue 7 , June 2010 , pp. 1139 - 1149
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Acero, S., Blanco, R. and Bartolomé, B. (2003). Anaphylaxis due to a tick bite. Allergy 58, 824–831. doi: 10.1034/j.1398-9995.2003.00211.CrossRefGoogle ScholarPubMed
Akerstrom, B., Flower, D. R. and Salier, J.-P. (2000). Lipocalins: unity in diversity. Biochimica et Biophysica Acta 1482, 1–8. doi:10.1016/S0167-4838(00)00137-0.CrossRefGoogle ScholarPubMed
Alarcon-Chaidez, F. J., Sun, J. and Wikel, S. K. (2007). Transcriptome analysis of the salivary glands of Dermacentor andersoni stiles (Acari: Ixodidae). Insect Biochemistry and Molecular Biology 37, 48–71. doi:10.1016/j.ibmb.2006.10.002.CrossRefGoogle ScholarPubMed
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Howe, K. L. and Sonnhammer, E. L. L. (2000). The Pfam protein families database. Nucleic Acids Research 28, 263–266.CrossRefGoogle ScholarPubMed
Beaufays, J., Adam, B., Decrem, Y., Prévôt, P.-P., Santini, S., Brasseur, R., Brossard, M., Lins, L., Vanhamme, L. and Godfroid, E. (2008). Ixodes ricinus tick lipocalins: Identification, cloning, phylogenetic analysis and biochemical characterization. Plos One 3, e3941. doi: 10.1371/journal.pone.0003941.CrossRefGoogle ScholarPubMed
Bendtsen, J. D., Nielsen, H., von Heijne, G. and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340, 783–795. doi:10.1016/j.jmb.2004.05.028.CrossRefGoogle ScholarPubMed
Blom, N., Gammeltoft, S. and Brunak, S. (1999). Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of Molecular Biology 294, 1351–1362. doi:10.1006/jmbi.1999.3310.CrossRefGoogle ScholarPubMed
Bork, P., Holm, L. and Sander, C. (1994). The immunoglobulin fold. Structural classification, sequence patterns and common core. Journal of Molecular Biology 242, 309–320. doi:10.1006/jmbi.1994.1582.Google ScholarPubMed
Čeřovský, V., Hovorka, O., Cvačka, J., Voburka, Z., Bednárová, L., Borovičková, L., Slaninová, J. and Fučík, V. (2008). Melectin: a novel antimicrobial peptide from the venom of the cleptoparasitic bee Melecta albifrons. ChemBioChem 24, 2815–2821. doi: 10.1002/cbic.200800476.CrossRefGoogle Scholar
Chmelař, J., Anderson, J. M., Mu, J., Jochim, R. C., Valenzuela, J. G. and Kopecký, J. (2008). Insight into the sialome of the castor bean tick, Ixodes ricinus. BMC Genomics 9, 233. doi:10.1186/1471-2164-9-233.CrossRefGoogle ScholarPubMed
Derewenda, U., Li, J., Derewenda, Z., Dauter, Z, Mueller, G. A., Rule, G. S. and Benjamin, D. C. (2002). The crystal structure of a major dust mite allergen Der p 2, and its biological implications. Journal of Molecular Biology 318, 189–197. doi:10.1016/S0022-2836(02)00027-X.CrossRefGoogle Scholar
Francischetti, I. M., Sá-Nunes, A., Mans, B. J., Santos, I. M. and Ribeiro, J. M. (2009). The role of saliva in tick feeding. Frontiers in Bioscience 14, 2051–2088. doi:10.2741/3363.CrossRefGoogle ScholarPubMed
Friedland, N., Liou, H.-L., Lobel, P. and Stock, A. M. (2003). Structure of a cholesterol-binding protein deficient in Niemann–Pick type C2 disease. Proceedings of the National Academy of Sciences, USA 100, 2512–2517. doi: 10.1073/pnas.0437840100.CrossRefGoogle ScholarPubMed
Hilger, C., Bessot, J.-C., Hutt, N., Grigioni, F., de Blay, F., Pauli, G. and Hentges, F. (2005). IgE-mediated anaphylaxis caused by bites of the pigeon tick Argas reflexus: Cloning and expression of the major allergen Arg r 1. Journal of Allergy and Clinical Immunology 115, 617–622. doi:10.1016/j.jaci.2004.11.052.CrossRefGoogle ScholarPubMed
Ichikawa, S., Hatanaka, H., Yuuki, T., Iwamoto, N., Kojima, S., Nishiyama, C., Ogura, K., Okumura, Y. and Inagaki, F. (1998). Solution structure of Der f 2, the major mite allergen for atopic diseases. The Journal of Biological Chemistry 273, 356–360.CrossRefGoogle ScholarPubMed
Ichikawa, S., Takai, T., Inoue, T., Yuuki, T., Okumura, Y., Ogura, K., Inagaki, F. and Hatanaka, H. (2005). NMR study on the major mite allergen Der f 2: Its refined tertiary structure, epitopes for monoclonal antibodies and characteristics shared by ML protein group members. The Journal of Biochemistry 137, 255–263. doi: 10.1093/jb/mvi039.CrossRefGoogle Scholar
Inohara, N. and Nuñez, G. (2002). ML – a conserved domain involved in innate immunity and lipid metabolism. Trends in Biochemical Science 27, 219–221. doi:10.1016/S0968-0004(02)02084-4.CrossRefGoogle Scholar
Julenius, K., Mølgaard, A., Gupta, R. and Brunak, S. (2005). Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15, 153–164. doi:10.1093/glycob/cwh151.CrossRefGoogle ScholarPubMed
Keller, P. M., Waxman, L., Arnold, B. A., Schultz, L. D., Condra, C. and Connolly, T. M. (1993). Cloning of the cDNA and expression of moubatin, an inhibitor of platelet aggregation. The Journal of Biological Chemistry 268, 5450–5456.CrossRefGoogle ScholarPubMed
Lawrie, C. H. and Nuttall, P. A. (2001). Antigenic profile of Ixodes ricinus: effect of developmental stage, feeding time and the response of different host species. Parasite Immunology 23, 549–556.CrossRefGoogle ScholarPubMed
Lawson, D., Arensburger, P., Atkinson, P., Besansky, N. J., Bruggner, R. V., Butler, R., Campbell, K. S., Christophides, G. K., Christley, S., Dialynas, E., Hammond, M., Hill, C. A., Konopinski, N., Lobo, N. F., MacCallum, R. M., Madey, G., Megy, K., Meyer, J., Redmond, S., Severson, D. W., Stinson, E. O., Topalis, P., Birney, E., Gelbart, W. M., Kafatos, F. C., Louis, C. and Collins, F. H. (2009). VectorBase: a data resource for invertebrate vector genomics. Nucleic Acids Research 37, D583–D587. doi: 10.1093/nar/gkn857.CrossRefGoogle ScholarPubMed
Leboulle, G., Rochez, C., Louahed, J., Rutti, B., Bollen, A. and Godfroid, E. (2002). Isolation of Ixodes ricinus salivary gland mRNA encoding factors induced during blood feeding. American Journal of Tropical Medicine and Hygiene 66, 225–233.CrossRefGoogle ScholarPubMed
Mahuran, D. J. (1998). The GM2 activator protein, its roles as a co-factor in GM2 hydrolysis and as a general glycolipid transport protein. Biochimica et Biophysica Acta 1393, 1–18. doi:10.1016/S0005-2760(98)00057-5.CrossRefGoogle ScholarPubMed
Mans, B. J., Andersen, J. F., Francischetti, I. M. B., Valenzuela, J. G., Schwan, T. G., Pham, V. M., Garfield, M. K., Hammer, C. H. and Ribeiro, J. M. C. (2008). Comparative sialomics between hard and soft ticks: Implications for the evolution of blood-feeding behavior. Insect Biochemistry and Molecular Biology 38, 42–58. doi:10.1016/j.ibmb.2003.09.002.CrossRefGoogle ScholarPubMed
Mans, B. J., Louw, A. I. and Neitz, A. W. (2003). The major tick salivary gland proteins and toxins from the soft tick, Ornithodoros savignyi, are part of the tick lipocalin family: implications for the origins of tick toxicoses. Molecular Biology and Evolution 20, 1158–1167. doi: 10.1093/molbev/msg126.CrossRefGoogle ScholarPubMed
Mans, B. J. and Neitz, A. W. H. (2004). Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochemistry and Molecular Biology 34, 1–17.CrossRefGoogle ScholarPubMed
Marchler-Bauer, A., Anderson, J. B., Derbyshire, M. K., DeWeese-Scott, C., Gonzales, N. R., Gwadz, M., Hao, L., He, S., Hurwitz, D. I., Jackson, J. D., Ke, Z., Krylov, D., Lanczycki, C. J., Liebert, C. A., Liu, C., Lu, F., Lu, S., Marchler, G. H., Mullokandov, M., Song, J. S., Thanki, N., Yamashita, R. A., Yin, J. J., Zhang, D. and Bryant, S. H. (2007). CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Research 35, 237–240. doi: 10.1093/nar/gkl951.CrossRefGoogle ScholarPubMed
Marchler-Bauer, A. and Bryant, S. H. (2004). CD-Search: protein domain annotations on the fly. Nucleic Acids Research 32, W327–W331. doi: 10.1093/nar/gkh454.CrossRefGoogle ScholarPubMed
McGuffin, L. J., Bryson, K. and Jones, D. T. (2000). The PSIPRED protein structure prediction server. Bioinformatics 16, 404–405.CrossRefGoogle ScholarPubMed
Mueller, G. A, Benjamin, D. C. and Rule, G. S. (1998). Tertiary structure of the major house dust mite allergen Der p 2: Sequential and structural homologies. Biochemistry 37, 12707–12714. doi: 10.1021/bi980578.CrossRefGoogle ScholarPubMed
Mullen, G. E. D., Kennedy, M. N., Visintin, A., Mazzoni, A., Leifer, C. A., Davies, D. R. and Segal, D. M. (2003). The role of disulfide bonds in the assembly and function of MD-2. Proceedings of the National Academy of Sciences, USA 100, 3919–3924. doi: 10.1073/pnas.0630495100.CrossRefGoogle ScholarPubMed
Ohto, U., Fukase, K., Miyake, K. and Satow, Y. (2007). Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316, 1632–1634. doi: 10.1126/science.1139111.CrossRefGoogle ScholarPubMed
Paesen, G. C., Adams, P. L., Harlos, K., Nuttall, P. A. and Stuart, D. I. (1999). Tick histamine-binding proteins: Isolation, cloning, and three-dimensional structure. Molecular Cell 3, 661–671. doi:10.1016/S1097-2765(00)80359-7.CrossRefGoogle ScholarPubMed
Porollo, A. and Meller, J. (2007). Versatile annotation and publication quality visualization of protein complexes using POLYVIEW-3D. BMC Bioinformatics 8, 316. doi: 10.1186/1471-2105-8-316.CrossRefGoogle ScholarPubMed
Quackenbush, J., Cho, J., Lee, D., Liang, F., Holt, I., Karamycheva, S., Parvizi, B., Pertea, G., Sultana, R. and White, J. (2001). The TIGR gene indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Research 29, 159–164.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. C. (1995). How ticks make a living. Parasitology Today 3, 91–93. doi:10.1016/0169-4758(95)80162-6.CrossRefGoogle Scholar
Rolla, G., Nebiolo, F., Marsico, P., Guida, G., Bigo, P., Riva, G. and Zanotta, S. (2004). Allergy to pigeon tick (Argas reflexus): Demonstration of specific IgE-binding components. International Archives of Allergy and Immunology 135, 293–295. doi: 10.1159/000082322.CrossRefGoogle ScholarPubMed
Rudenko, N., Golovchenko, M., Edwards, M. J. and Grubhoffer, L. (2005). Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. Journal of Medical Entomology 42, 36–41.CrossRefGoogle ScholarPubMed
Sangamnatdej, S., Paesen, G. C., Slovak, M. and Nuttall, P. A. (2002). A high affinity serotonin- and histamine-binding lipocalin from tick saliva. Insect Molecular Biology 11, 79–86. doi: 10.1046/j.0962-1075.2001.00311.CrossRefGoogle ScholarPubMed
Schultz, J., Milpetz, F., Bork, P. and Ponting, C. P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences, USA 95, 5857–5864.CrossRefGoogle Scholar
Shimazu, R., Akashi, S., Ogata, H., Nagai, Y., Fukudome, K., Miyake, K. and Kimoto, M. (1999). MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. Journal of Experimental Medicine 189, 1777–1782.CrossRefGoogle ScholarPubMed
Shin, K. H., Jeong, K. Y., Hong, C.-S. and Yong, T.-S. (2009). IgE binding reactivity of peptide fragments of Bla g 4, a major german cockroach allergen. The Korean Journal of Parasitology 47, 31–36. doi: 10.3347/kjp.2009.47.1.31.CrossRefGoogle Scholar
Sonenshine, D. E. and Hynes, W. L. (2008). Molecular characterization and related aspects of the innate immune response in ticks. Frontiers in Bioscience 13, 7046–7063. doi: 10.2741/3209.CrossRefGoogle ScholarPubMed
Thomas, W. R., Smith, W.-A., Hales, B. J., Mills, K. L. and O'Brien, R. M. (2002). Characterization and immunobiology of house dust mite allergens. International Archieves of Allergy and Immunology 129, 1–18. doi: 10.1159/000065179.CrossRefGoogle ScholarPubMed
Wang, H., Paesen, G. C., Nuttall, P. A. and Barbour, A. (1998). Male ticks help their mates to feed. Nature, London 391, 753–754.CrossRefGoogle ScholarPubMed
Wang, H. and Nuttall, P. A. (1999). Immunoglobulin-binding proteins in ticks: new target for vaccine development against a blood-feeding parasite. Cellular and Molecular Life Sciences 56, 286–2895.CrossRefGoogle ScholarPubMed
Wright, C. S., Li, S.-C. and Rastinejad, F. (2000). Crystal structure of human GM2-activator protein with a novel β-cup topology. Journal of Molecular Biology 304, 411–422. doi:10.1006/jmbi.2000.4225.CrossRefGoogle ScholarPubMed
Wright, C. S., Mi, L. Z., Lee, S. and Rastinejad, F. (2005). Crystal structure analysis of phosphatidylcholine-GM2-activator product complexes: evidence for hydrolase activity. Biochemistry 44, 13510–13521. doi: 10.1021/bi050668w.CrossRefGoogle ScholarPubMed