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Identification and localization of a putative ATP-binding cassette transporter in sea lice (Lepeophtheirus salmonis) and host Atlantic salmon (Salmo salar)

Published online by Cambridge University Press:  26 October 2007

N. D. TRIBBLE
Affiliation:
Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PEI, CanadaC1A 4P3
J. F. BURKA*
Affiliation:
Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PEI, CanadaC1A 4P3
F. S. B. KIBENGE
Affiliation:
Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PEI, CanadaC1A 4P3
G. M. WRIGHT
Affiliation:
Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PEI, CanadaC1A 4P3
*
*Corresponding author: Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, 550 University Ave., Charlottetown, PEI, CanadaC1A 4P3. Tel: +1 902 566 0810. Fax: +1 902 566 0832. E-mail: burka@upei.ca

Summary

Some members of the ABC-transporter superfamily, such as P-glycoprotein and the multidrug resistance associated protein, may confer resistance to the avermectin subclass of macrocyclic lactones. The aim of this study was to examine the presence of ABC transporters in both sea lice (Lepeophtheirus salmonis) and its Atlantic salmon host (Salmo salar) using monoclonal antibodies (C219 and JSB-1, with high selectivity for P-gp) and a new polyclonal antibody (SL0525) generated against a putative sea louse ABC transporter. The antibody raised to SL0525 did not react with rat P-gp, suggesting that an ABC transporter, not necessarily P-gp, was isolated. C219 was the only antibody to localize P-gp in all 3 salmon tissues (intestine, kidney and liver). American lobster (Homarus americanus) was used as a reference crustacean for L. salmonis immunostaining reactions and showed positive staining in the hepatopancreatic and intestinal tissues with all 3 antibodies. The L. salmonis showed positive staining in the intestinal epithelial lining with all antibodies. This report represents the first documented evidence for the expression of ABC transporters in L. salmonis, its Atlantic salmon host, and the American lobster.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Al-Mohanna, S. Y., Nott, J. A. and Lane, D. J. W. (1985). Mitotic E and secretory F-cells in the hepatopancreas of the shrimp Penaeus semisulcatus (Crustacea: Decapoda). Journal of the Marine Biological Association of the United Kingdom 65, 901910.Google Scholar
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403410.Google Scholar
Ardelli, B. F., Guerriero, S. B. and Prichard, R. K. (2005). Genomic organization and effects of ivermectin selection on Onchocerca volvulus P-glycoprotein. Molecular and Biochemical Parasitology 143, 5866.Google Scholar
Ardelli, B. F., Guerriero, S. B. and Prichard, R. K. (2006 a). Ivermectin imposes selection pressure on P-glycoprotein from Onchocerca volvulus: linkage disequilibrium and genotype diversity. Parasitology 132, 375386.Google Scholar
Ardelli, B. F., Guerriero, S. B. and Prichard, R. K. (2006 b). Characterization of a half-size ATP-binding cassette transporter gene which may be a useful marker for ivermectin selection in Onchocerca volvulus. Molecular and Biochemical Parasitology 145, 94100.Google Scholar
Blackhall, W. J., Liu, H. Y., Xu, M., Prichard, R. K. and Beech, R. N. (1998). Selection at a P-glycoprotein gene in ivermectin- and moxidectin-selected strains of Haemonchus contortus. Molecular and Biochemical Parasitology 95, 193201.Google 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
Burridge, L. E., Hamilton, N., Waddy, S. L., Haya, K., Mercer, S. M., Greenhalgh, R., Tauber, R., Radecki, S. V., Crouch, L. S., Wislocki, P. G. and Endris, R. G. (2004). Acute toxicity of emamectin benzoate (SLICE™) in fish feed to American lobster, Homarus americanus. Aquaculture Research 35, 713722.Google Scholar
Cascorbi, I. (2006). Role of pharmacogenetics of ATP-binding cassette transporters in the pharmacokinetics of drugs. Pharmacology and Therapeutics 112, 457473.Google Scholar
Coers, W., Timens, W., Kempinga, C., Klok, P. A. and Moshage, H. (1998). Specificity of antibodies to nitric oxide synthase isoforms in human, guinea pig, rat, and mouse tissues. Journal of Histochemistry and Cytochemistry 46, 13851391.Google Scholar
Fikrig, E., Barthold, S. W., Kantor, F. S. and Flavell, R. A. (1990). Protection of mice against the Lyme disease agent by immunizing with recombinant OspA. Science 250, 553556.Google Scholar
Frangioni, J. V. and Neel, B. G. (1993). Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Analytical Biochemistry 210, 179187.Google Scholar
Fulton, M. H., Moore, D. W., Wirth, E. F., Chandler, G. T., Key, P. B., Daugomah, J. W., Strozier, E. D., Devane, J., Clark, J. R., Lewis, M. A., Finley, D. B., Ellenberg, W., Karnaky, K. J. J. and Scott, G. I. (1999). Assessment of risk reduction strategies for the management of agricultural non point source pesticide runoff in estuarine ecosystems. Toxicology and Industrial Health 15, 200213.Google Scholar
Georges, E., Bradley, G., Gariepy, J. and Ling, V. (1990). Detection of P-glycoprotein isoforms by gene-specific monoclonal antibodies. Proceedings of the National Academy of Sciences, USA 87, 152156.Google Scholar
Hemmer, M. J., Courtney, L. A. and Benson, W. H. (1998). Comparison of three histological fixatives on the immunoreactivity of mammalian P-glycoprotein antibodies in the sheepshead minnow, Cyprinodon variegatus. Journal of Experimental Zoology 281, 251259.Google Scholar
Hemmer, M. J., Courtney, L. A. and Ortego, L. S. (1995). Immunohistochemical detection of P-glycoprotein in teleost tissues using mammalian polyclonal and monoclonal antibodies. Journal of Experimental Zoology 272, 6977.Google Scholar
Kerr, I. D. (2004). Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochemical and Biophysical Research Communications 315, 166173.Google Scholar
Kibenge, F. S. B., Lyaku, J. R., Rainnie, D. J. and Hammell, K. L. (2000). Growth of infectious salmon anaemia virus in CHSE-214 cells and evidence for phenotypic differences between virus strains. Journal of General Virology 81, 143150.Google Scholar
Kim-Kang, H., Bova, A., Crouch, L. S., Wislocki, P. G., Robinson, R. A. and Wu, J. (2004). Tissue distribution, metabolism, and residue depletion study in Atlantic salmon following oral administration of [3H] emamectin benzoate. Journal of Agricultural and Food Chemistry 52, 21082118.Google Scholar
Kumar, S., Tamura, K. and Nei, M. (1994). MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Computer Applications in the Biosciences 10, 189191.Google Scholar
Liu, B., Sun, D., Xia, W., Hung, M. C. and Yu, D. (1997). Cross-reactivity of C219 and anti-p170 (MDR-1) antibody with p185 (C-erbB2) in breast cancer cells: cautions on evaluating p170 (mdr-1). Journal of the National Cancer Institute 89, 15241529.Google Scholar
Loo, T. W., Bartlett, M. C. and Clarke, D. M. (2002). The “LSGGQ” motif in each nucleotide-binding domain of human P-glycoprotein is adjacent to the opposing walker A sequence. Journal of Biological Chemistry 277, 4130341306.Google Scholar
Lyons-Alcantara, M., Lambkin, H. A., Nordmo, R., Lyng, F. and Mothersill, C. (2002). Cross-reactivity of some antibodies to human epitopes with shrimp Pandalus borealis proteins: a possible aid in validation and characterization of crustacean cells in vitro. Cell Biochemistry and Function 20, 247256.Google Scholar
Martin, R. J., Robertson, A. P. and Wolstenholme, A. J. (2002). Mode of action of macrocyclic lactones. In: Macrocyclic Lactones in Antiparasitic Therapy (ed. Vercruysse, J. and Rew, R. S.), pp. 125140. CABI Publishing, Oxford.Google Scholar
Minier, C., Akcha, F. and Galgani, F. (1993). P-glycoprotein expression in Crassostrea gigas and Mytilus edulis in polluted seawater. Comparative Biochemistry and Physiology 106, 10291036.Google Scholar
Pike, A. W. and Wadsworth, S. L. (1999). Sea lice on salmonids: their biology and control. Advances in Parasitology 44, 233337.Google Scholar
Qian, F., Wei, D., Liu, J. and Yang, S. (2006). Molecular model and ATPase activity of carboxyl-terminal nucleotide binding domain from human P-glycoprotein. Biochemistry 71, 1820.Google Scholar
Rao, V. V., Antony, D. C. and Piwnica-Worms, D. (1995). Multidrug resistance P-glycoprotein monoclonal antibody JSB-1 crossreacts with pyruvate carboxylase. Journal of Histochemistry and Cytochemistry 43, 11871192.Google Scholar
Schering Plough Animal Health (2007). Product and Disease Directory: SLICE ®Premix. Available online at: http://www.spaquaculture.com/default.aspx?pageid=545Google Scholar
Sevatdal, S., Magnusson, A., Ingebrigtsen, K., Haldorsen, R. and Horsberg, T. E. (2005). Distribution of emamectin benzoate in Atlantic salmon (Salmo salar L.). Journal of Veterinary Pharmacology and Therapeutics 28, 101107.Google Scholar
Smital, T. and Kurelec, B. (1998). The chemosensitizers of multixenobiotic resistance mechanism in aquatic invertebrates: a new class of pollutants. Mutation Research 399, 4353.Google Scholar
Smith, J. M. and Prichard, R. K. (2002). Localization of P-glycoprotein mRNA in the tissues of Haemonchus contortus adult worms and its relative abundance in drug-selected and susceptible strains. Journal of Parasitology 88, 612620.Google Scholar
Sousa, L. G., Cuartas, E. I. and Petriella, A. M. (2005). Fine structural analysis of the epithelial cells in the hepatopancreas of Palaemonetes argentinus (Crustacea, Decapoda, Caridea) in intermoult. Biocell 29, 2531.Google Scholar
Stone, J., Sutherland, I. H., Sommerville, C., Richards, R. H. and Varma, K. J. (2000). Commercial trials using emamectin benzoate to control sea lice Lepeophtheirus salmonis infestations in Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 41, 141149.Google Scholar
Sturm, A., Ziemann, C., Hirsch-Ernst, K. I. and Segner, H. (2001). Expression and functional activity of P-glycoprotein in cultured hepatocytes from Oncorhynchus mykiss. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 281, 11191126.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.Google Scholar
Tribble, N. D., Burka, J. F. and Kibenge, F. S. B. (2007). Evidence for changes in the transcription levels of two putative P-glycoprotein genes in sea lice (Lepeophtheirus salmonis) in response to emamectin benzoate exposure. Molecular Biochemistry and Parasitology 153, 5965.Google Scholar
Volk, H., Potschka, H. and Loscher, W. (2005). Immunohistochemical localization of P-glycoprotein in rat brain and detection of its increased expression by seizures are sensitive to fixation and staining variables. Journal of Histochemistry and Cytochemistry 53, 517531.Google Scholar
Westcott, J. D., Hammell, K. L. and Burka, J. F. (2004). Sea lice treatments, management practices and sea lice sampling methods on Atlantic salmon farms in the Bay of Fundy, New Brunswick, Canada. Aquaculture Research 35, 784792.Google Scholar
Xu, M., Molento, M., Blackhall, W. J., Ribeiro, P., Beech, R. N. and Prichard, R. K. (1998). Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Molecular and Biochemical Parasitology 91, 327335.Google Scholar