Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-24T03:58:49.429Z Has data issue: false hasContentIssue false

Assessment of cathepsin D and L-like proteinases of poultry red mite, Dermanyssus gallinae (De Geer), as potential vaccine antigens

Published online by Cambridge University Press:  06 February 2012

KATHRYN BARTLEY*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ, Scotland, UK
JOHN F. HUNTLEY
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ, Scotland, UK
HARRY W. WRIGHT
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ, Scotland, UK
MINTU NATH
Affiliation:
Biomathematics and Statistics Scotland, James Clerk Maxwell Building, The King's Buildings, Edinburgh EH9 3JZ, Scotland, UK
ALASDAIR J. NISBET
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ, Scotland, UK
*
*Corresponding author: Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ, Scotland, UK. Tel: +44 (0)131 445 5111. Fax: +44 (0)131 445 6235. E-mail: [email protected]

Summary

Vaccination is a feasible strategy for controlling the haematophagous poultry red mite Dermanyssus gallinae. A cDNA library enriched for genes upregulated after feeding was created to identify potential vaccine antigens. From this library, a gene (Dg-CatD-1) encoding a 383 amino acid protein (Dg-CatD-1) with homology to cathepsin D lysosomal aspartyl proteinases was identified as a potential vaccine candidate. A second gene (Dg-CatL-1) encoding a 341 amino acid protein (Dg-CatL-1) with homology to cathepsin L cysteine proteinases was also selected for further study. IgY obtained from naturally infested hens failed to detect Dg-CatD-1 suggesting that it is a concealed antigen. Conversely, Dg-CatL-1 was detected by IgY derived from natural-infestation, indicating that infested hens are exposed to Dg-CatL-1. Mortality rates 120 h after mites had been fed anti-Dg-CatD-1 were significantly higher than those fed control IgY (PF<0·01). In a survival analysis, fitting a proportional hazards model to the time of death of mites, anti-Dg-CatD-1 and anti-Dg-CatL-1 IgY had 4·42 and 2·13 times higher risks of dying compared with controls (PF<0·05). Dg-CatD-1 and L-1 both have potential as vaccine antigens as part of a multi-component vaccine and have the potential to be improved as vaccine antigens using alternative expression systems.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Bartley, K., Nisbet, A. J., Offer, J., Sparks, N., Wright, H. and Huntley, J. F. (2009). Histamine Release Factor from Dermanyssus gallinae (De Geer): Characterisation and in vitro assessment as a protective antigen. International Journal for Parasitology 39, 447456.CrossRefGoogle Scholar
Benjamini, Y. and Hochberg, Y. (1995). Controlling the False Discovery Rate - A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57, 289300.Google Scholar
Bethony, J. M., Cole, R. N., Guo, X., Kamhawi, S., Lightowlers, M. W., Loukas, A., Petri, W., Reed, S., Valenzuela, J. G. and Hotez, P. J. (2011). Vaccines to combat the neglected tropical diseases. Immunological Reviews 239, 237270.CrossRefGoogle ScholarPubMed
Britton, C. and Murray, L. (2006). Using Caenorhabditis elegans for functional analysis of genes of parasitic nematodes. International Journal for Parasitology 36, 651659.CrossRefGoogle ScholarPubMed
Chauve, C. (1998). The poultry red mite Dermanyssus gallinae (De Geer, 1778): current situation and future prospects for control. Veterinary Parasitology 79, 239245.CrossRefGoogle Scholar
Dalton, J. P., Neill, S. O., Stack, C., Collins, P., Walshe, A., Sekiya, M., Doyle, S., Mulcahy, G., Hoyle, D., Khaznadji, E., Moire, N., Brennan, G., Mousley, A., Kreshchenko, N., Maule, A. G. and Donnelly, S. M. (2003). Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. International Journal for Parasitology 33, 11731181.CrossRefGoogle ScholarPubMed
da Silva Vas, I. Jr., Logullo, C., Sorgine, M., Velloso, F. F., Rosa de Lima, M. F., Gonzales, J. C., Masuda, H., Oliveira, P. L. and Masuda, A. (1998). Immunization of bovines with an aspartic proteinase precursor isolated from Boophilus microplus eggs. Veterinary Immunology Immunopathology 66, 331341.CrossRefGoogle Scholar
de Castro, E., Sigrist, C. J. A., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P. S., Gasteiger, E., Bairoch, A. and Hulo, N. (2006). ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Research 34 (Web Server issue), W362-5.CrossRefGoogle ScholarPubMed
de la Fuente, J. and Kocan, K. M. (2006). Strategies for development of vaccines for control of ixodid tick species. Parasite Immunology 28, 275283.CrossRefGoogle ScholarPubMed
de la Fuente, J. and Kocan, K. M. (2003). Advances in the identification and characterisation of protective antigens for recombinant vaccines against tick infestations. Expert Review of Vaccines 2, 583593.CrossRefGoogle ScholarPubMed
Dowling, D. J., Hamilton, C. M., Donnelly, S., La Course, J., Brophy, P. M., Dalton, J. and O'Neill, S. M. (2010). Major secretory antigens of the helminth Fasciola hepatica activate suppressive dendritic cell phenotype that attenuates Th17 cells but fails to activate Th2 immune responses. Infection and Immunology 78, 793801.CrossRefGoogle ScholarPubMed
Emanuelsson, O., Brunak, S., von Heijne, G. and Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2, 953971.CrossRefGoogle ScholarPubMed
Estrela, A. B., Seixas, A., Teixeira, V. O., Pinto, A. F. and Termignoni, C. (2010). Vitellin- and hemoglobin-digesting enzymes in Rhipicephalus (Boophilus) microplus larvae and females. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 157, 326335.CrossRefGoogle ScholarPubMed
Gupta, R. and Brunak, S. (2002). Prediction of glycosylation across the human proteome and the correlation to protein function. Pacific Symposium on Biocomputing 7, 310322.Google Scholar
Harrington, D., Canales, M., de la Fuente, J., de Luna, C., Robinson, K., Guy, J. and Sparagano, O. (2009 a). Immunisation with recombinant proteins subolesin and Bm86 for the control of Dermanyssus gallinae in poultry. Vaccine 27, 40564063.CrossRefGoogle ScholarPubMed
Harrington, D., Din, H. M., Guy, J., Robinson, K. and Sparagano, O. (2009 b). Characterisation of the immune response of domestic fowl following immunization with proteins extracted from Dermanyssus gallinae. Veterinary Parasitology 160, 285294.CrossRefGoogle ScholarPubMed
Harrington, D., Robinson, K., Guy, J. and Sparagano, O. (2010). Characterization of the immunological response to Dermanyssus gallinae infestation in domestic fowl. Transboundary and Emerging Diseases 57, 107110.CrossRefGoogle ScholarPubMed
Jasinskas, A., Jaworski, D. C. and Barbour, A. G. (2000). Amblyomma americanum: specific uptake of immunoglobulins into tick hemolymph during feeding. Experimental Parasitology 96, 213221.CrossRefGoogle ScholarPubMed
Jayaraj, R., Piedrafita, D., Dynon, K., Grams, R., Spithill, T. W. and Smooker, P. M. (2009). Vaccination against fasciolosis by a multivalent vaccine of stage-specific antigens. Veterinary Parasitology 160, 230236.CrossRefGoogle ScholarPubMed
Jeffers, L. A. and Roe, M. R. (2008). The movement of proteins across the insect and tick digestive system. Journal of Insect Physiology 54, 319332.CrossRefGoogle ScholarPubMed
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, 153164.CrossRefGoogle ScholarPubMed
Karrer, K. M., Peiffer, S. L. and DiTomas, M. E. (1993). Two distinct gene subfamilies within the family of cysteine protease genes. Proceedings of the National Academy of Sciences, USA 90, 30633067.CrossRefGoogle ScholarPubMed
Kemp, D. H., Pearson, R. D., Gough, J. M. and Willadsen, P. (1989). Vaccination against Boophilus microplus: localization of antigens on tick gut cells and their interaction with the host immune system. Experimental and Applied Acarology 7, 4358.CrossRefGoogle ScholarPubMed
Knox, D. P., Redmond, D. L., Newlands, G. F., Skuce, P. J., Pettit, D. and Smith, W. D. (2003). The nature and prospects for gut membrane proteins as vaccine candidates for Haemonchus contortus and other ruminant trichostrongyloids. International Journal for Parasitology 33, 11291137.CrossRefGoogle ScholarPubMed
Knox, D. P., Smith, S. K., Redmond, D. L. and Smith, W. D. (2005). Protection induced by vaccinating sheep with a thiol-binding extract of Haemonchus contortus membranes is associated with its protease components. Parasite Immunology 27, 121126.CrossRefGoogle ScholarPubMed
Leal, A. T., Seixas, A., Pohl, P. C., Ferreira, C. A., Logullo, C., Oliveira, P. L., Farias, S. E., Termignoni, C., da Silva Vas, I. Jr and Masuda, A. (2006). Vaccination of bovines with recombinant Boophilus yolk pro-Cathepsin. Veterinary Immunology and Immunopathology 114, 341345.CrossRefGoogle ScholarPubMed
Longbottom, D., Redmond, D. L., Russell, M., Liddell, S., Smith, W. D. and Knox, D. P. (1997). Molecular cloning and characterisation of a putative aspartate proteinase associated with a gut membrane complex from adult Haemonchus contortus. Molecular and Biochemical Parasitology 88, 6372.CrossRefGoogle ScholarPubMed
Marangi, M., Cafiero, M. A., Capelli, G., Camarda, A., Sparagano, O. A. and Giangaspero, A. (2009). Evaluation of the poultry red mite, Dermanyssus gallinae (Acari: Dermanyssidae) susceptibility to some acaricides in field populations from Italy. Experimental and Applied Acarology 48, 1118.CrossRefGoogle ScholarPubMed
McDevitt, R., Nisbet, A. J. and Huntley, J. F. (2006). Ability of a proteinase inhibitor cocktail to kill poultry red mite, Dermanyssus gallinae in an in vitro feeding system. Veterinary Parasitology 141, 380385.CrossRefGoogle Scholar
Mulenga, A., Sugimoto, C., Ingram, G., Ohashi, K. and Onuma, M. (1999). Molecular cloning of two Haemaphysalis longicornis cathepsin L-like cysteine proteinase genes. Journal of Veterinary Medical Science 61, 497502.CrossRefGoogle ScholarPubMed
Murray, L., Geldhof, P., Clark, D., Knox, D. P. and Britton, C. (2007). Expression and purification of an active cysteine protease of Haemonchus contortus using Caenorhabditis elegans. International Journal for Parasitology 37, 11171125.CrossRefGoogle ScholarPubMed
Nisbet, A. J. and Billingsley, P. F. (2000). A comparative survey of the hydrolytic enzymes of parasitic and free-living mites. International Journal for Parasitology. 30, 1928.CrossRefGoogle ScholarPubMed
Nisbet, A. J. and Huntley, J. F. (2006). Progress and opportunities in the development of vaccines against mites, fleas and myiasis-causing flies of veterinary importance. Parasite Immunology 28, 165172.CrossRefGoogle ScholarPubMed
Nisbet, A. J., Huntley, J. F., MacKellar, A., Sparks, N. and McDevitt, R. (2006). A house dust mite allergen homologue from poultry red mite Dermanyssus gallinae (De Geer). Parasite Immunology 28, 401404.CrossRefGoogle ScholarPubMed
Nisbet, A. J., Redmond, D. L., Matthews, J. B., Watkins, C., Yaga, R., Jones, J. T., Nath, M. and Knox, D. P. (2008). Stage-specific gene expression in Teladorsagia circumcincta (Nematoda: Strongylida). International Journal for Parasitology 38, 829838.CrossRefGoogle ScholarPubMed
Pearson, M. S., Ranjit, N. and Loukas, A. (2010). Blunting the knife: development of vaccines targeting digestive proteases of blood-feeding helminth parasites. Biological Chemistry 391, 901911.CrossRefGoogle ScholarPubMed
Pettit, D., Smith, W. D., Richardson, J. and Munn, E. A. (2000). Localisation and characterisation of ovine immunglobulin within the sheep scab mite, Psoroptes ovis. Veterinary Parasitology 89, 231239.CrossRefGoogle ScholarPubMed
Rawlings, N. D. and Barrett, A. J. (1993). Evolutionary families of peptidases. The Biochemical Journal 240, 205218.CrossRefGoogle Scholar
R Development Core Team (2011). A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Release 2.13. http://www.R-project.org.Google Scholar
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, 10171026.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. Insect Molecular Biology 11, 325328.CrossRefGoogle ScholarPubMed
Rost, B., Yachdav, G. and Liu, J. (2004). The PredictProtein Server. Nucleic Acids Research 32 (Web Server issue):W321-6.CrossRefGoogle ScholarPubMed
Seixas, A., Dos Santos, P. C., Velloso, F. F., da Silva Vas, I. Jr, Masuda, A., Horn, F. and Termignoni, C. (2003). A Boophilus microplus vitellin-degrading cysteine endopeptidase. Parasitology 126, 155163.CrossRefGoogle ScholarPubMed
Seixas, A., Estrela, A. B., Ceolato, J. C., Pontes, E. G., Lara, F., Gondim, K. C. and Termignoni, C. (2010). Localization and function of Rhipicephalus (Boophilus) microplus vitellin-degrading cysteine endopeptidase. Parasitology 137, 18191831.CrossRefGoogle ScholarPubMed
Seixas, A., Leal, A. T., Nascimento-Silva, M. C., Masuda, A., Termignoni, C. and da Silva Vas, I. Jr (2008). Vaccine potential of a tick vitellin-degrading enzyme (VTDCE). Veterinary Immunology and Immunopathology 124, 332–40.CrossRefGoogle ScholarPubMed
Sigrist, C. J. A., Cerutti, L., de Castro, E., Langendijk-Genevaux, P. S., Bulliard, V., Bairoch, A. and Hulo, N. (2010). PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Research 38 (Database issue), 161–6.CrossRefGoogle ScholarPubMed
Smith, W. D., Skuce, P. J., Newlands, G. F., Smith, S. K. and Pettit, D. (2003). Aspartyl proteases from the intestinal brush border of Haemonchus contortus as protective antigens for sheep. Parasite Immunology 25, 521530.CrossRefGoogle ScholarPubMed
Tellam, R. L., Kemp, D., Riding, G., Briscoe, S., Smith, D., Sharp, P., Irving, D. and Willadsen, P. (2002). Reduced oviposition of Boophilus microplus feeding on sheep vaccinated with vitellin. Veterinary Parasitology 103, 141156.CrossRefGoogle ScholarPubMed
Valiente Moro, C., De Luna, C. J., Tod, A., Guy, J. H., Sparagano, O. A. and Zenner, L. (2009). The poultry red mite (Dermanyssus gallinae): a potential vector of pathogenic agents. Experimental and Applied Acarology 48, 93104.CrossRefGoogle ScholarPubMed
Van Emous, R. (2005). Wage war against the red mite! Poultry International 44, 2633.Google Scholar
Vernet, T., Berti, P. J., de, M. C., Musil, R., Tessier, D. C., Menard, R., Magny, M. C., Storer, A. C. and Thomas, D. Y. (1995). Processing of the papain precursor. The ionization state of a conserved amino acid motif within the Pro region participates in the regulation of intramolecular processing. Journal of Biological Chemistry 270, 1083810846.CrossRefGoogle ScholarPubMed
Willadsen, P. (2004). Anti-tick vaccines. Parasitology 129 (Suppl.) S367S387.CrossRefGoogle ScholarPubMed
Wright, H. W., Bartley, K., Nisbet, A. J., McDevitt, R., Sparks, N., Brocklehurst, S. and Huntley, J. F. (2009). The testing of antibodies raised against poultry red mite antigens in an in vitro feeding assay; preliminary screen for vaccine candidates. Experimental and Applied Acarology 48, 8191.CrossRefGoogle Scholar
Yamaji, K., Tsuji, N., Miyoshi, T., Islam, M. K., Hatta, T., Alim, M. A., Anisuzzaman, ▪., Takenaka, A. and Fujisaki, K. (2009). Hemoglobinase activity of a cysteine protease from the ixodid tick Haemaphysalis longicornis. Parasitology International 58, 232237.CrossRefGoogle ScholarPubMed