Hostname: page-component-7bb8b95d7b-qxsvm Total loading time: 0 Render date: 2024-09-11T11:19:18.572Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular characterization, expression and localization of a peroxiredoxin from the sheep scab mite, Psoroptes ovis

Published online by Cambridge University Press:  06 February 2009

C. M. McNAIR ,
A. J. NISBET ,
P. F. BILLINGSLEY  and
D. P. KNOX
C. M. McNAIR
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, Scotland
A. J. NISBET
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, Scotland
P. F. BILLINGSLEY
Affiliation:
Sanaria Inc., 12115 Parklawn Drive, Ste L, Rockville, MD 20852-1730, USA
D. P. KNOX*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, Scotland
*
*Corresponding author: Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, Scotland. Tel: +44 (0)131 445 5111. Fax: +44 (0)131 445 6235. E-mail: Dave.Knox@moredun.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The sheep scab mite, Psoroptes ovis, induces an intensely pruritic exudative dermatitis which is responsible for restlessness, loss of appetite and weight loss. Within the first 24 h of infection, there is a rapid inflammatory influx of eosinophils and apoptosis of the keratinocytes at the site of infection. The former cell type is capable of a sustained respiratory burst, toxic products of which may directly damage the mite and also contribute to lesion formation. Analysis of a P. ovis expressed sequence tag (EST) database identified a number of antioxidant enzyme-encoding sequences, including peroxiredoxin (thioredoxin peroxidase EC 1.11.1.15), all of which may help the mite endure the potentially toxic skin environment. A full length sequence encoding Po-TPx, a protein of 206 amino acids which showed high homology to a peroxiredoxin from the salivary gland of the tick Ixodes scapularis, was amplified from P. ovis cDNA. Recombinant Po-TPx was expressed in bacteria and antiserum to this protein was used to localize native Po-TPx in mite sections. Peroxiredoxin was localized, amongst other sites, to a subpharyngeal region in mite sections. The recombinant protein was recognized by sera from sheep infested with the mite suggesting that it may be secreted or excreted by the mite and interact with the host immune response.

Keywords

Psoroptes ovisantioxidantimmunityreactive oxygen species
Type
Research Article
Information
Parasitology , Volume 136 , Issue 4 , April 2009 , pp. 453 - 460
Copyright
Copyright © 2009 Cambridge University Press

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

Akov, S. (1982). Blood digestion in ticks. In Physiology of Ticks (ed. Obenchain, F. D. and Galun, R.), pp. 197–211. Pergamon Press, Oxford, UK.Google Scholar
Chae, H. Z., Chung, S. J. and Rhee, S. G. (1994). Thioredoxin-dependent peroxide reductase from yeast. Journal of Biological Chemistry 269, 27670–27678.CrossRefGoogle ScholarPubMed
Clark, A. M., Stephen, F. B., Cawley, G. D., Bellworthy, S. J. and Groves, B. A. (1996). Resistance of the sheep scab mite Psoroptes ovis to propetamphos. Veterinary Record 139, 451.Google Scholar
Das, S., Banerjee, G., DePonte, K., Marcantonio, N., Kantor, F. S. and Fikrig, E. (2001). Salp25D, an Ixodes scapularis antioxidant, is 1 of 14 immunodominant antigens in engorged tick salivary glands. Journal of Infectious Diseases 184, 1056–1064.CrossRefGoogle ScholarPubMed
Donnelly, S., O'Neill, S. M., Sekiya, M., Mulcahy, G. and Dalton, J. P. (2005). Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infection and Immunity 73, 166–173.Google Scholar
Dyrløv Bendtsen, J., Nielsen, H., von Heijne, G. and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340, 783–795.CrossRefGoogle Scholar
Hovius, J. W., Levi, M. and Fikrig, E. (2008). Salivating for knowledge: potential pharmacological agents in tick saliva. PLoS Medicine 5, e43.CrossRefGoogle ScholarPubMed
Huntley, J. F., van den Broek, A., Machell, J., Mackellar, A., Pettit, D., Meikle, L., Barcham, G., Meeusen, E. N. and Smith, W. D. (2005). The effect of immunosuppression with cyclosporin A on the development of sheep scab. Veterinary Parasitology 127, 323–332.CrossRefGoogle ScholarPubMed
James, P. J. (1999). Do sheep regulate the size of their mallophagan louse populations? International Journal for Parasitology 29, 869–875.CrossRefGoogle ScholarPubMed
James, P. J., Moon, R. D. and Ragsdale, D. W. (1998). Skin surface antibodies and their associations with sheep biting lice, Bovicola ovis, on experimentally infested sheep. Medical and Veterinary Entomology 12, 276–283.Google Scholar
Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. and Gibson, T. J. (1998). Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23, 403–405.CrossRefGoogle ScholarPubMed
Jenkinson, D. M. E. (1989). Skin surface responses to external challenge. In Practice 11, 207–209.CrossRefGoogle Scholar
Kenyon, F., Welsh, M., Parkinson, J., Whitton, C., Blaxter, M. L. and Knox, D. P. (2003). Expressed sequence tag survey of gene expression in the scab mite Psoroptes ovis – allergens, proteinases and free radical scavengers. Parasitology 126, 451–460.CrossRefGoogle ScholarPubMed
Kuchler, K. and Thorner, J. (1992). Secretion of peptides and proteins lacking hydrophobic signal sequences: the role of adenosine triphosphate-driven membrane translocators. Endocrinological Reviews 13, 499–514.Google Scholar
Liddell, S. and Knox, D. P. (1998). Extracellular and cytoplasmic Cu/Zn superoxide dismutases from Haemonchus contortus. Parasitology 116, 383–394.CrossRefGoogle ScholarPubMed
Lim, M. J., Chae, H. Z., Rhee, S. G., Yu, D. Y., Lee, K. K. and Yeom, Y. I. (1998). The type II peroxiredoxin gene family of the mouse: molecular structure, expression and evolution. Gene 216, 197–205.CrossRefGoogle ScholarPubMed
LoVerde, P. T. (1998). Do antioxidants play a role in Schistosome host-parasite interactions? Parasitology Today 14, 284–289.Google Scholar
Lo Verde, P. T., Carvalho-Queiroz, C.Cook, R. (2004). Vaccination with antioxidant enzymes confers protective immunity against challenge infection with Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz 99, 37–43.CrossRefGoogle ScholarPubMed
Mathieson, B. R. (1995). An investigation of Psoroptes ovis, the sheep scab mite, with a view to developing an in vitro feeding system. Ph.D. thesis, University of Aberstywyth, Wales, UK.Google Scholar
Nieuwhof, G. J. and Bishop, S. C. (2005). Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science 81, 23–29.CrossRefGoogle Scholar
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, 165–172.Google Scholar
Nisbet, A. J., Halliday, A. M., Parker, L., Smith, W. D., Kenyon, F., Knox, D. P. and Huntley, J. F. (2008). Psoroptes ovis: identification of vaccine candidates by immunoscreening. Experimental Parasitology 120, 194–199.CrossRefGoogle ScholarPubMed
Pettit, D., Smith, W. D., Richardson, J. and Munn, E. A. (2000). Localisation and characterisation of ovine immunoglobulin within the sheep scab mite, Psoroptes ovis. Veterinary Parasitology 89, 231–239.Google Scholar
Ribeiro, J. M., Alarcon-Chaidez, F., Francischetti, I. M., Mans, B. J., Mather, T. N., Valenzuela, J. G. and Wikel, S. K. (2006). An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochemistry and Molecular Biology 36, 111–129.CrossRefGoogle ScholarPubMed
Shalaby, K. A., Yin, L., Thakur, A., Christen, L., Niles, E. G. and LoVerde, P. T. (2003). Protection against Schistosoma mansoni utilizing DNA vaccination with genes encoding Cu/Zn cytosolic superoxide dismutase, signal peptide-containing superoxide dismutase and glutathione peroxidase enzymes. Vaccine 22, 130–136.CrossRefGoogle ScholarPubMed
Smith, W. D. and Pettit, D. M. (2004). Immunization against sheep scab: preliminary identification of fractions of Psoroptes ovis which confer protective effects. Parasite Immunology 26, 307–314.Google Scholar
Synge, B. A., Bates, P. G., Clark, A. M. and Stephen, F. B. (1995). Apparent resistance to flumethrin. Veterinary Record 137, 51.CrossRefGoogle ScholarPubMed
Tauber, A. I., Goetzl, E. J. and Babior, B. M. (1979). Unique characteristics of superoxide production by human eosinophils in eosinophilic states. Inflammation 3, 261–272.CrossRefGoogle ScholarPubMed
Tsuji, N., Kamio, T., Isobe, T. and Fujisaki, K. (2001). Molecular characterization of a peroxiredoxin from the hard tick Haemaphysalis longicornis. Insect Molecular Biology 10, 121–129.CrossRefGoogle ScholarPubMed
Vaca-Paniagua, F., Torres-Rivera, A., Parra-Unda, R. and Landa, A. (2008). Taenia solium: antioxidant metabolism enzymes as targets for cestocidal drugs and vaccines. Current Topics in Medicinal Chemistry 8, 393–399.Google ScholarPubMed
van den Broek, A. H., Huntley, J. F., MacHell, J., Taylor, M., Bates, P., Groves, B. and Miller, H. R. (2000). Cutaneous and systemic responses during primary and challenge infestations of sheep with the sheep scab mite, Psoroptes ovis. Parasite Immunology 22, 407–414.CrossRefGoogle ScholarPubMed