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Localization and function of Rhipicephalus (Boophilus) microplus vitellin-degrading cysteine endopeptidase

Published online by Cambridge University Press:  21 June 2010

ADRIANA SEIXAS ,
ANDRÉIA B. ESTRELA ,
JULIANA C. CEOLATO ,
EMERSON G. PONTES ,
FLÁVIO LARA ,
KATIA C. GONDIM  and
CARLOS TERMIGNONI
ADRIANA SEIXAS*
Affiliation:
Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
ANDRÉIA B. ESTRELA
Affiliation:
Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
JULIANA C. CEOLATO
Affiliation:
Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
EMERSON G. PONTES
Affiliation:
Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
FLÁVIO LARA
Affiliation:
Departamento de Bioquímica, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil Pavilhão Hanseníase, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil
KATIA C. GONDIM
Affiliation:
Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
CARLOS TERMIGNONI
Affiliation:
Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil Departamento de Bioquímica, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
*
*Corresponding author: Avenida Bento Gonçalves 9500, Prédio 43431, Sala 217, Campus do Vale, Caixa Postal 15005, CEP 91501-970, Porto Alegre, RS, Brazil. Tel: +55 51 33086082. Fax: +55 51 33087309. E-mail: adriana@cbiot.ufrgs.br
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Summary

The tick Rhipicephalus (Boophilus) microplus is an important parasite of cattle in many areas of the tropics. Characterization of molecules involved in mechanisms such as vitellogenesis and embryo development may contribute to a better understanding of this parasite's physiology. The vitellin-degrading cysteine endopeptidase (VTDCE) is the most active enzyme involved in vitellin hydrolysis in R. microplus eggs. Here we show an association between VTDCE and vitellin in an additional site, apart from the active site. Our data also demonstrate cysteine endopeptidase activity in different tissues such as ovary, gut, fat body, salivary gland and female haemolymph, where it is controlled by a physiological inhibitor. In R. microplus female gut, VTDCE is localized in areas of protein synthesis and trafficking with the underlying haemolymph. VTDCE is also localized in the ovary basal region, in vesicle membranes of ovary pedicel cells and in oocyte cytosol. These results suggest that VTDCE plays a role in vitellin digestion during tick development.

Keywords

Rhipicephalus (Boophilus) micropluscysteine endopeptidasecysteine endopeptidase inhibitorhaemolymphvitellinVTDCE
Type
Research Article
Information
Parasitology , Volume 137 , Issue 12 , October 2010 , pp. 1819 - 1831
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Agbede, R. I. and Kemp, D. H. (1987). Boophilus microplus (ixodid tick): fine structure of the gut basophilic cell in relation to water and ion transport. Experimental and Applied Acarology 3, 233–242.CrossRefGoogle ScholarPubMed
Balashov, Y. S. (1983). The female reproductive system. In An Atlas of Ixodid Tick Ultrastructure (ed. Balashov, Y. S.), pp. 98–128. Entomology Society of America, College Park, USA.CrossRefGoogle Scholar
Carnevali, O., Cionna, C., Tosti, L., Lubzens, E. and Maradonna, F. (2006). Role of cathepsins in ovarian follicle growth and maturation. Genetics Comparative Endocrinology 146, 195–203.CrossRefGoogle ScholarPubMed
Cho, W.-L., Tsao, S.-M., Hays, A. R., Walter, R., Chen, J.-S., Snigirevskaya, E. S. and Raikhel, A. S. (1999). Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. Journal of Biological Chemistry 19, 13311–13321.CrossRefGoogle Scholar
Coons, L. B., Tarnowski, B. and Ourth, D. D. (1982). Rhipicephalus sanguinius: localization of vitellogenin synthesis by immunological methods and electron microscopy. Experimental Parasitology 54, 331–339.CrossRefGoogle ScholarPubMed
Cristofoletti, P. T., Ribeiro, A. F. and Terra, W. R. (2005). The cathepsin L-like proteinases from the midgut of Tenebrio molitor larvae: sequence, properties, immunocytochemical localization and function. Insect Biochemistry and Molecular Biology 35, 883–901.CrossRefGoogle ScholarPubMed
de la Fuente, J., Almazan, C., Canales, M., Perez de la Lastra, J. M.P., Kocan, K. M. and Willadsen, P. (2007). A ten-year review of commercial vaccine performance for control of tick infestations on cattle. Animal Health Research Review 8, 23–28.CrossRefGoogle ScholarPubMed
Estrela, A., Seixas, A. and Termignoni, C. (2007). A cysteine endopeptidase from tick (Rhipicephalus (Boophilus) microplus) larvae with vitellin digestion activity. Comparative Biochemistry and Physiology - Part B 148, 410–416.CrossRefGoogle ScholarPubMed
Fagotto, F. (1990). Yolk degradation in tick eggs: I. Occurrence of a cathepsin L- like acid proteinase in yolk spheres. Archives of Insect Biochemistry and Physiology 14, 217–235.CrossRefGoogle ScholarPubMed
Fagotto, F. (1995). Regulation of yolk degradation, or how to make sleepy lysosomes. Journal of Cell Sciences 108, 3645–3647.CrossRefGoogle ScholarPubMed
Frame, M. J., Mottram, J. C. and Coombs, G. H. (2000). Analysis of the roles of cysteine proteinases of Leishmania mexicana in the host-parasite interaction. Parasitology 121, 367–377.CrossRefGoogle ScholarPubMed
Giorgi, F., Bradley, J. T. and Nordin, J. H. (1999). Differential vitellin polypeptide processing in insect embryos. Micron 30, 579–596.CrossRefGoogle Scholar
Glauert, A. M. (1974). The right voltage electron microscope in biology. Journal of Cell Biology 63, 717–748.CrossRefGoogle Scholar
Gondim, K. C. and Wells, M. (2000). Characterization of lipophorin binding to the gut of larval Manduca sexta. Insect Biochemistry and Molecular Biology 30, 405–413.CrossRefGoogle Scholar
Horn, F., dos Santos, P. and Termignoni, C. (2000). Boophilus microplus anticoagulant protein: an antithrombin inhibitor isolated from the cattle tick saliva. Archives of Biochemistry and Biophysics 384, 68–73.CrossRefGoogle ScholarPubMed
Horn, M., Nussbaumerová, M., Sanda, M., Kovárová, Z., Srba, J., Franta, Z., Sojka, D., Bogyo, M., Caffrey, C. R., Kopácek, P. and Mares, M. (2009). Hemoglobin digestion in blood-feeding ticks: mapping a multipeptidase pathway by functional proteomics. Chemical Biology 16, 1053–1063.CrossRefGoogle ScholarPubMed
Kucera, M. and Turner, R. B. (1981). Purification and properties of protease inhibitors from developing embryos of Hemileuca oliviae. Biochimica et Biophysica Acta 611, 379–383.Google Scholar
Krasko, A., Gamulin, V., Seack, J., Steffen, R., Schroder, H. C. and Muller, W. E. (1997). Cathepsin, a major protease of the marine sponge Geodia cydonium: purification of the enzyme and molecular cloning of cDNA. Molecular Marine Biology Biotechnology 6, 296–307.Google ScholarPubMed
Lima, C. A., Sasaki, S. D. and Tanaka, A. S. (2006). Bmcystatin, a cysteine proteinase inhibitor characterized from the tick Boophilus microplus. Biochemical and Biophysical Research Communications 18, 44–50.CrossRefGoogle Scholar
Logullo, C., da Silva Vaz, I. Jr., Sorgine, M. H., Paiva-Silva, G. O., Faria, F. S., Zingali, R. B., De Lima, M. F., Abreu, L., Oliveira, E. F., Alves, E. W., Masuda, H., Gonzales, J. C., Masuda, A. and Oliveira, P. L. (1998). Isolation of an aspartic proteinase precursor from the egg of a hard tick, Boophilus microplus. Parasitology 116, 525–532.CrossRefGoogle ScholarPubMed
Logullo, C., Moraes, J., Dansa-Petretski, M., Vaz, I. S., Masuda, A., Sorgine, M. H., Braz, G. R., Masuda, H. and Oliveira, P. L. (2002). Binding and storage of heme by vitellin from the cattle tick, Boophilus microplus. Insect Biochemistry and Molecular Biology 32, 1805–1811.CrossRefGoogle ScholarPubMed
Mendiola, J., Alonso, M., Marquetti, M. C. and Finlay, C. (1996). Boophilus microplus: multiple proteolytic activities in the midgut. Experimental Parasitology 82, 27–33.CrossRefGoogle ScholarPubMed
McGrath, M. E. (1999). The lysosomal cysteine proteases. Annual Review of Biophysics and Biomolecular Structure 28, 181–204.CrossRefGoogle ScholarPubMed
Meirelles, M. N. L., Juliano, L., Carmona, E., Silva, S. G., Costa, E. M., Murta, A. C. M. and Scharfstein, J. (1992). Inhibitors of the major cysteinyl proteinase (Gp57/51) impair host-cell invasion and arrest the intracellular development of Trypanosoma cruzi invitro. Molecular and Biochemical Parasitology 52, 175–184.CrossRefGoogle Scholar
Mitchell, R. D. 3rd, Ross, E., Osgood, C., Sonenshine, D. E., Donohue, K. V., Khalil, S. M., Thompson, D. M. and Michael Roe, R. (2007). Molecular characterization, tissue-specific expression and RNAi knockdown of the first vitellogenin receptor from a tick. Insect Biochemistry and Molecular Biology 37, 375–388.CrossRefGoogle ScholarPubMed
Nascimento-Silva, M. C., Leal, A. T., Daffre, S., Juliano, L., da Silva Vaz, I. Jr, Paiva-Silva, G. de O., Oliveira, P. L. and Sorgine, M. H. (2008). BYC, an atypical aspartic endopeptidase from Rhipicephalus (Boophilus) microplus eggs. Comparative Biochemistry and Physiology – Part B 149, 599–607.CrossRefGoogle ScholarPubMed
Nordin, J. H., Beaudoin, E. L. and Liu, X. D. (1990). Proteolytic processing of Blattella germanica vitellin during early embryo development. Archives of Insect Biochemistry and Physiology 15, 119–135.CrossRefGoogle Scholar
Oliveira, M. C., Hirata, I. Y., Chagas, J. R., Boschcov, P., Gomes, R. A., Figueiredo, A. F. and Juliano, L. (1992). Intramolecularly quenched fluorogenic peptide substrates for human renin. Analytical Biochemistry 203, 39–46.CrossRefGoogle ScholarPubMed
Raikhel, A. S. and Dhadialla, T. S. (1992). Accumulation of yolk proteins in insect oocytes. Annual Review of Entomololgy 37, 217–251.CrossRefGoogle ScholarPubMed
Renard, G., Garcia, J. F., Cardoso, F. C., Richter, M. F., Sakanari, J. A., Ozaki, L. S., Termignoni, C. and Masuda, A. (2000). Cloning and functional expression of a Boophilus microplus cathepsin L-like enzyme. Insect Biochemistry and Molecular Biology 30, 1017–1026.CrossRefGoogle ScholarPubMed
Renard, G., Lara, F. A., de Cardoso, F. C., Miguens, F. C., Dansa-Petretski, M., Termignoni, C. and Masuda, A. (2002). Expression and immunolocalization of a Boophilus microplus cathepsin L-like enzyme. Molecular Biology 11, 325–328.Google ScholarPubMed
Ricardo, A. J., de Oliveira, P. R., Bechara, G. H. and Mathias, M. I. (2007). Ultrastructural detection of proteins, lipids and carbohydrates in oocytes of Amblyomma triste (Koch, 1844) (Acari; Ixodidae) during the vitellogenesis process. Tissue and Cell 39, 203–215.CrossRefGoogle ScholarPubMed
Saito, K. C., Bechara, G. H., Nunes, E. T., de Oliveira, P. R., Denardi, S. E. and Mathias, M. I. (2005). Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Veterinary Parasitology 129, 299–311.CrossRefGoogle ScholarPubMed
Sajid, M. and McKerrow, J. H. (2002). Cysteine proteases of parasitic organisms. Molecular and Biochemical Parasitology 120, 1–21. Erratum in: Molecular and Biochemical Parasitology (2002) 30, 121–159.CrossRefGoogle ScholarPubMed
Seixas, A., Dos Santos, P. C., Velloso, F. F., da Silva, V. I. Jr., Masuda, A., Horn, F. and Termignoni, C. (2003). A Boophilus microplus vitellin-degrading cysteine endopeptidase. Parasitology 126, 155–163.CrossRefGoogle ScholarPubMed
Seixas, A., Leal, A. T., Nascimento-Silva, M. C., Masuda, A., Termignoni, C. and da Silva Vaz, I. Jr. (2008). Vaccine potential of a tick vitellin-degrading enzyme (VTDCE). Veterinary Immunology and Immunopathology 124, 332–340.CrossRefGoogle ScholarPubMed
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J. and Klenk, D. C. (1985). Measurement of protein using bicinchonic acid. Analytical Biochemistry 150, 76–85.CrossRefGoogle Scholar
Sojka, D., Franta, Z., Horn, M., Hajdusek, O., Caffrey, C. R., Mares, M. and Kopacek, P. (2008). Profiling of proteolytic enzymes in the gut of the tick Ixodes ricinus reveals an evolutionarily conserved network of aspartic and cysteine peptidases. Parasite & Vectors 1, 7. doi:10.1186/1756-3305-1-7CrossRefGoogle ScholarPubMed
Sonenshine, D. E. (1991). Biology of Ticks, Vol. 1. Oxford University Press, Oxford, UK.Google Scholar
Till, W.M. (1961). A Contribution to the Anatomy and Histology of the Brown Ear Tick Rhipicephalus appendiculatus. Swets & Zeitlinger Publishers, Amsterdam, The Netherlands.Google Scholar
Willadsen, P. (2006). Vaccination against ectoparasites. Parasitology 133, (Suppl.) S9-S25.CrossRefGoogle ScholarPubMed
Willadsen, P. (2004). Anti-tick vaccines. Parasitology 129, (Suppl.) S367–387.CrossRefGoogle ScholarPubMed
Yin, L., Nordin, J. H., Lucches, P. and Giorgi, F. (2001). Cysteine proprotease colocalizes with vitellogenin in compound granules of the cockroach fat body. Cell and Tissue Research 304, 391–399.CrossRefGoogle ScholarPubMed
Yu, D., Wang, D. Y.C. C. and Wang, A. L. (1995). Maturation of giardiavirus capsid protein involves posttranslational proteolytic processing by a cysteine protease. Journal of Virology 69, 2825–2830.CrossRefGoogle ScholarPubMed