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Effect of acaricides on the activity of glutathione transferases from the parasitic mite Sarcoptes scabiei

Published online by Cambridge University Press:  10 September 2007

E. U. MOLIN
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agricultural Sciences, SE-751 89 Uppsala, Sweden
J. G. MATTSSON*
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agricultural Sciences, SE-751 89 Uppsala, Sweden
*
*Corresponding author. Tel: +46 18 67 40 00. Fax: +46 18 67 43 04. E-mail: Jens.Mattsson@sva.se

Summary

Glutathione transferases (GSTs) are a family of multifunctional enzymes with fundamental roles in cellular detoxication. Here we report the molecular characterization of 3 recombinant GSTs belonging to the mu- and delta-class from the parasitic mite Sarcoptes scabiei. Kinetic constants were determined, and the effect of acaricides, including organothiophosphates, pyrethroid esters, a formamidine, a macrocyclic lactone, an organochlorine as well as a bridged diphenyl acaricide, on the activity of the GSTs were tested using 1-chloro-2,4-dinitrobenzene (CDNB) as model substrate. Our results showed that enzymes from the same class and with high amino acid sequence identity have significantly different kinetic properties. For instance, one mu-class GST lost more than 50% of its activity in the presence of one of the organothiophosphates while the activity of the second mu-class GST was only slightly reduced under identical conditions. Tertiary structure modulations indicated that structural differences were the crucial factor for the different kinetic patterns observed. Genome analysis showed that the two mu-class GSTs are organized in tandem in the S. scabiei genome. Taken together these results show that GSTs might be involved in the metabolism of acaricides in S. scabiei.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Angelucci, F., Baiocco, P., Brunori, M., Gourlay, L., Morea, V. and Bellelli, A. (2005). Insights into the catalytic mechanism of glutathione S-transferase: the lesson from Schistosoma haematobium. Structure 13, 12411246. DOI: 10.1016/j.str.2005.06.007.CrossRefGoogle ScholarPubMed
Bornstein, S. and Zakrisson, G. (1993). Humoral antibody response to experimental Sarcoptes scabiei var. vulpes infection in the dog. Veterinary Dermatology 4, 107110.CrossRefGoogle Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.Google Scholar
Burgess, I. (1994). Sarcoptes scabiei and scabies. Advances in Parasitology 33, 235292.Google Scholar
Currie, B. J., Harumal, P., McKinnon, M. and Walton, S. F. (2004). First documentation of in vivo and in vitro ivermectin resistance in Sarcoptes scabiei. Clinical Infectious Diseases 39, e812. DOI: 10.1086/421776.CrossRefGoogle ScholarPubMed
da Silva Vaz, I.Torino Lermen, T. Jr., Michelon, A., Sanchez Ferreira, C. A., Joaquim de Freitas, D. R., Termignoni, C. and Masuda, A. (2004 a). Effect of acaricides on the activity of a Boophilus microplus glutathione S-transferase. Veterinary Parasitology 119, 237245.CrossRefGoogle ScholarPubMed
da Silva Vaz, I. Jr.Imamura, S., Ohashi, K. and Onuma, M. (2004 b). Cloning, expression and partial characterization of a Haemaphysalis longicornis and a Rhipicephalus appendiculatus glutathione S-transferase. Insect Molecular Biology 13, 329335. DOI: 10.1111/j.0962-1075.2004.00493.x.Google Scholar
Donabedian, H. and Khazan, U. (1992). Norwegian scabies in a patient with AIDS. Clinical Infectious Diseases 14, 162164.Google Scholar
Dougall, A., Holt, D. C., Fischer, K., Currie, B. J., Kemp, D. J. and Walton, S. F. (2005). Identification and characterization of Sarcoptes scabiei and Dermatophagoides pteronyssinus glutathione S-transferases: implication as a potential major allergen in crusted scabies. The American Journal of Tropical Medicine and Hygiene 73, 977984.Google Scholar
Enayati, A. A., Ranson, H. and Hemingway, J. (2005). Insect glutathione transferases and insecticide resistance. Insect Molecular Biology 14, 38. DOI: 10.1111/j.1365-2583.2004.00529.x.Google Scholar
Feyereisen, R. (1995). Molecular biology of insecticide resistance. Toxicology Letters 82–83, 8390.Google Scholar
Firkins, L. D., Jones, C. J., Keen, D. P., Arends, J. J., Thompson, L., King, V. L. and Skogerboe, T. L. (2001). Preventing transmission of Sarcoptes scabiei var. suis from infested sows to nursing piglets by a prefarrowing treatment with doramectin injectable solution. Veterinary Parasitology 99, 323330. DOI: 10.1016/S0304-4017(01)00473-3.CrossRefGoogle ScholarPubMed
Fischer, K., Holt, D. C., Harumal, P., Currie, B. J., Walton, S. F. and Kemp, D. J. (2003). Generation and characterization of cDNA clones from Sarcoptes scabiei var. hominis for an expressed sequence tag library: identification of homologues of house dust mite allergens. The American Journal of Tropical Medicine and Hygiene 68, 6164.CrossRefGoogle ScholarPubMed
Foil, L. D., Coleman, P., Eisler, M., Fragoso-Sanchez, H., Garcia-Vazquez, Z., Guerrero, F. D., Jonsson, N. N., Langstaff, I. G., Li, A. Y., Machila, N., Miller, R. J., Morton, J., Pruett, J. H. and Torr, S. (2004). Factors that influence the prevalence of acaricide resistance and tick-borne diseases. Veterinary Parasitology 125, 163181. DOI: 10.1016/j.vetpar.2004.05.012.Google Scholar
Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 71307139.CrossRefGoogle ScholarPubMed
He, H., Chen, A. C., Davey, R. B., Ivie, G. W. and George, J. E. (1999). Characterization and molecular cloning of a glutathione S-transferase gene from the tick, Boophilus microplus (Acari: Ixodidae). Insect Biochemistry and Molecular Biology 29, 737743. DOI: 10.1006/bbrc.1999.1076.CrossRefGoogle ScholarPubMed
Hemingway, J. (2000). The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochemistry and Molecular Biology 30, 10091015.Google Scholar
Heukelbach, J. and Feldmeier, H. (2006). Scabies. The Lancet 367, 17671774. DOI: 10.1016/S0140-6736(06)68772-2.CrossRefGoogle ScholarPubMed
Jirajaroenrat, K., Pongjaroenkit, S., Krittanai, C., Prapanthadara, L. and Ketterman, A. J. (2001). Heterologous expression and characterization of alternatively spliced glutathione S-transferases from a single Anopheles gene. Insect Biochemistry and Molecular Biology 31, 867875.CrossRefGoogle ScholarPubMed
Ketterman, A. J., Prommeenate, P., Boonchauy, C., Chanama, U., Leetachewa, S., Promtet, N. and Prapanthadara, L. (2001). Single amino acid changes outside the active site significantly affect activity of glutathione S-transferases. Insect Biochemistry and Molecular Biology 31, 6574.CrossRefGoogle ScholarPubMed
Kostaropoulos, I., Papadopoulos, A. I., Metaxakis, A., Boukouvala, E. and Papadopoulou-Mourkidou, E. (2001). Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochemistry and Molecular Biology 31, 313319.Google Scholar
Kumar, A. and Reddy, E. P. (2001). Genomic organization and characterization of the promoter region of murine GSTM2 gene. Gene 270, 221229.CrossRefGoogle ScholarPubMed
McCarthy, J. S., Kemp, D. J., Walton, S. F. and Currie, B. J. (2004). Scabies: more than just an irritation. Postgraduate Medical Journal 80, 382387. DOI: 10.1136/pgmj.2003.014563.Google Scholar
Morel, F., Rauch, C., Coles, B., Le Ferrec, E. and Guillouzo, A. (2002). The human glutathione transferase alpha locus: genomic organization of the gene cluster and functional characterization of the genetic polymorphism in the hGSTA1 promoter. Pharmacogenetics 12, 277286.Google Scholar
Mörner, T. (1992). Sarcoptic mange in Swedish wildlife. Revue Scientifique et Technique – Office International des Epizooties 11, 11151121.Google Scholar
Ortelli, F., Rossiter, L. C., Vontas, J., Ranson, H. and Hemingway, J. (2003). Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. The Biochemical Journal 373, 957963. DOI: 10.1042/BJ20030169.Google Scholar
Pettersson, E. U., Ljunggren, E. L., Morrison, D. A. and Mattsson, J. G. (2005). Functional analysis and localisation of a delta-class glutathione S-transferase from Sarcoptes scabiei. International Journal for Parasitology 35, 3948. DOI: 10.1016/j.ijpara.2004.09.006.Google Scholar
Sharp, P. J., Smith, D. R., Bach, W., Wagland, B. M. and Cobon, G. S. (1991). Purified glutathione S-transferases from parasites as candidate protective antigens. International Journal for Parasitology 21, 839846.CrossRefGoogle ScholarPubMed
Sheehan, D., Meade, G., Foley, V. M. and Dowd, C. A. (2001). Structure, function and evolution of glutathione transferases: Implications for classification of non-mammalian members of an ancient enzyme superfamily. The Biochemical Journal 360, 116.Google Scholar
Soranzo, N., Sari Gorla, M., Mizzi, L., De Toma, G. and Frova, C. (2004). Organisation and structural evolution of the rice glutathione S-transferase gene family. Molecular Genetics and Genomics 271, 511521. DOI: 10.1007/s00438-004-1006-8.Google Scholar
Walton, S. F., Currie, B. J. and Kemp, D. J. (1997). A DNA fingerprinting system for the ectoparasite Sarcoptes scabiei. Molecular and Biochemical Parasitology 85, 187196.Google Scholar
Walton, S. F., Holt, D. C., Currie, B. J. and Kemp, D. J. (2004). Scabies: new future for a neglected disease. Advances in Parasitology 57, 309376. DOI: 10.1016/S0065-308x(04)57005-7.Google Scholar
Widersten, M., Björnestedt, R. and Mannervik, B. (1996). Involvement of the carboxyl groups of glutathione in the catalytic mechanism of human glutathione transferase A1-1. Biochemistry 35, 77317742. DOI: 10.1021/bi9601619.Google Scholar