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Inventory and analysis of ATP-binding cassette (ABC) systems in Brugia malayi

Published online by Cambridge University Press:  17 March 2010

B. F. ARDELLI*
Affiliation:
Department of Biology, Brodie Science Building, Brandon University, 270-18th Street, Brandon, Manitoba, Canada R7A 6A9
L. E. STITT
Affiliation:
Department of Biology, Brodie Science Building, Brandon University, 270-18th Street, Brandon, Manitoba, Canada R7A 6A9
J. B. TOMPKINS
Affiliation:
Department of Biology, Brodie Science Building, Brandon University, 270-18th Street, Brandon, Manitoba, Canada R7A 6A9
*
*Corresponding author: Tel: +1 204 571 8563. Fax: +1 204 728 7346. E-mail: [email protected]

Summary

ABC systems are one of the largest described protein superfamilies. These systems have a domain organization that may contain 1 or more transmembrane domains (ABC_TM1F) and 1 or 2 ATP-binding domains (ABC_2). The functions (e.g., import, export and DNA repair) of these proteins distinguish the 3 classes of ABC systems. Mining and PCR-based cloning were used to identify 33 putative ABC systems from the Brugia malayi genome. There were 31 class 2 genes, commonly called ABC transporters, and 2 class 3 genes. The ABC transporters were divided into subfamilies. Three belonged to subfamily A, 16 to subfamily B, 5 to subfamily C, 1 to subfamily E and 3 to subfamilies F and G, respectively. None were placed in subfamilies D and H. Similar to other ABC systems, the ABC_2 domain of B. malayi genes was conserved and contained the Walker A and B motifs, the signature sequence/linker region and the switch region with the conserved histidine. The ABC_TM1F domain was less conserved. The relative abundance of ABC systems was quantified using real-time reverse transcription PCR and was significantly higher in female adults of B. malayi than in males and microfilaria, particularly those in subfamilies B and C, which are associated with drug resistance.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Ali, M. M., Mukhtar, M. M., Baraka, O. Z., Homeida, M. M., Kheir, M. M. and Mackenzie, C. D. (2002). Immunocompetence may be important in the effectiveness of Mectizan (ivermectin) in the treatment of human onchocerciasis. Acta Tropica 84, 4953. doi: 10.1016/S0001-706X(02)00117-1.CrossRefGoogle ScholarPubMed
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. doi:10.1016/j.molbiopara.2005.CrossRefGoogle ScholarPubMed
Ardelli, B. F., Guerriero, S. B. and Prichard, R. K. (2006 a). 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, 94–100. doi:10.1016/j.molbiopara.CrossRefGoogle ScholarPubMed
Ardelli, B. F., Guerriero, S. B. and Prichard, R. K. (2006 b). Ivermectin imposes selection pressure on P-glycoprotein from Onchocerca volvulus: linkage disequilibrium and genotype diversity. Parasitology 11, 112. doi:10.1017/S0031182005008991.Google Scholar
Ardelli, B. F. and Prichard, R. K. (2004). Identification of variant ABC transporter genes among Onchocerca volvulus collected from treated and untreated patients in Ghana, West Africa. Annals of Tropical Medicine and Parasitology 98, 371384. doi: 10.1179/000349804225003415.CrossRefGoogle ScholarPubMed
Ardelli, B. F. and Prichard, R. K. (2007). Reduced genetic polymorphism in an Onchocerca volvulus ABC transporter gene following treatment with ivermectin. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 12231232. doi:10.1016/j.trstmh.2005.CrossRefGoogle Scholar
Ardelli, B. F., Stitt, L. E., Tompkins, J. B. and Prichard, R. K. (2009). A comparison of the effects of ivermectin and moxidectin on the nematode Caenorhabditis elegans. Veterinary Parasitology 165, 96–108. doi:10.1016/j.vetpar.2009.06.CrossRefGoogle ScholarPubMed
Awadzi, K., Boakye, D. A., Edwards, G., Opoku, N. O., Attah, S. K., Osei-Atweneboana, M. Y., Lazdins-Helds, J. K., Ardrey, A. E., Addy, E. T., Quartey, B. T., Ahmed, K., Boatin, B. A. and Soumbey-Alley, E. W. (2004 a). An investigation of persistent microfilaridermias despite multiple treatments with ivermectin, in two onchocerciasis-endemic foci in Ghana. Annals of Tropical Medicine and Parasitology 98, 231249. doi: 10.1179/000349804225003253.CrossRefGoogle ScholarPubMed
Awadzi, K., Attah, S. K., Addy, E. T., Opoku, N. O., Quartey, B. T., Lazdins-Helds, J. K., Ahmed, K., Boatin, B. A., Boakye, D. A. and Edwards, G. (2004 b). Thirty-month follow-up of sub-optimal responders to multiple treatments with ivermectin, in two onchocerciasis-endemic foci in Ghana. Annals of Tropical Medicine and Parasitology 98, 359370. Doi: 10.1179/000349804225003442.CrossRefGoogle ScholarPubMed
Bauer, B. E., Wolfger, H. and Kuchler, K. (1999). Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochimica et Biophysica Acta 1461, 217236. doi:10.1016/S0005-2736(99)00160-1.CrossRefGoogle ScholarPubMed
Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Finn, R. D. and Sonnhammer, E. L. (1999). Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins. Nucleic Acids Research 27, 260262.CrossRefGoogle ScholarPubMed
Blackhall, W. J., Prichard, R. K. and Beech, R. N. (2008). P-glycoprotein selection in strains of Haemonchus contortus resistant to benzimidazoles. Veterinary Parasitology 152, 101107. doi:10.1016/j.vetpar.2007.CrossRefGoogle ScholarPubMed
Boos, W. and Lucht, J. M. (1996). Periplasmic binding protein-dependent ABC transporters. In Escherichia coli and Salmonella Cellular and Molecular Biology, 2nd Edn (ed. Neidhardt, F. C.), pp. 11751209, ASM Press, Washington, USA.Google Scholar
Borst, P., Evers, R., Kool, M. and Wijnholds, J. (1999). The multidrug resistance protein family. Biochimica et Biophysica Acta 1461, 347357. doi:10.1016/S0005-2736(99)00167-4.CrossRefGoogle ScholarPubMed
Bourguinat, C., Ardelli, B. F., Pion, S. D., Kamgno, J., Gardon, J., Duke, B. O., Boussinesq, M. and Prichard, R. K. (2008). P-glycoprotein-like protein, a possible genetic marker for ivermectin resistance selection in Onchocerca volvulus. Molecular and Biochemical Parasitology 158, 101111. doi:10.1016/j.molbiopara.2007.CrossRefGoogle ScholarPubMed
Braibant, M., Gilot, P. and Content, J. (2000). The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiology Reviews 24, 449467.CrossRefGoogle ScholarPubMed
Broccardo, C., Luciani, M. and Chimini, G. (1999). The ABCA subclass of mammalian transporters. Biochimica et Biophysica Acta 1461, 395404. doi:10.1016/S0005-2736(99)00170-4.CrossRefGoogle ScholarPubMed
Chow, L. M. C. and Volkman, S. K. (1998). Plasmodium and Leishmania: the role of mdr genes in mediating drug resistance. Experimental Parasitology 90, 135141. doi: 10.1006/expr.1998.4311.CrossRefGoogle ScholarPubMed
Dassa, E. (2003). Phylogenetic and functional classification of ABC (ATP-binding cassette) systems. In ABC Proteins: from Bacteria to Man (ed. Holland, I. B., Cole, S. P. C., Kuchler, K. and Higgins, C. F.), pp. 335. Academic Press, London, UK.CrossRefGoogle Scholar
Dassa, E. and Bouige, P. (2001). The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Research in Microbiology 152, 211229.CrossRefGoogle ScholarPubMed
Dassa, E., Hofnung, M., Paulsen, I. T. and Saier, M. H. Jr. (1999). The Escherichia coli ABC transporters: an update. Molecular Microbiology 32, 887889. doi:10.1046/j.1365-2958.1999.01392.xCrossRefGoogle ScholarPubMed
Dean, M., Rzhetsky, A. and Allikmets, R. (2001). The human ATP-binding cassette (ABC) transporter superfamily. Genome Research 11, 11561166. doi: 10.1101/gr.184901.CrossRefGoogle ScholarPubMed
Decottignies, A. and Goffeau, A. (1997). Complete inventory of the yeast ABC proteins. Nature Genetics 15, 137145. doi:10.1038/ng0297-137.CrossRefGoogle ScholarPubMed
Ewart, G. D., Cannell, D., Cox, G. B. and Howells, A. J. (1994). Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster – implications for structure-function relationships. Journal of Biological Chemistry 269, 1037010377.CrossRefGoogle ScholarPubMed
Fath, M. J. and Kolter, R. (1993). ABC transporters – bacterial exporters. Microbiology Reviews 57, 995–1017.CrossRefGoogle ScholarPubMed
Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D. and Bairoch, A. (2003). ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research 31, 37843788. doi: 10.1093/nar/gkg563.CrossRefGoogle ScholarPubMed
Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M. W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B. W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrín-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G., Williams, D. J., Zhang, Y., Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L. and Scott, A. L. (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 21, 317, 17561760. doi: 10.1126/science.1145406.CrossRefGoogle Scholar
Higgins, C. F. (1992). ABC transporters: from microorganisms to man. Annual Review of Cell Biology 8, 67–113. doi:10.1146/annurev.cb.08.110192.000435.CrossRefGoogle ScholarPubMed
Higgins, C. F. (2001). ABC transporters: physiology, structure and mechanism – an overview. Research in Microbiology 152, 205210.CrossRefGoogle ScholarPubMed
Hopfner, K. P. and Tainer, J. A. (2003). Rad 50/SMC proteins and ABC transporters: unifying concepts from high resolution structures. Current Opinion in Structural Biology 13, 249255. doi:10.1016/S0959-440X(03)00037-X.CrossRefGoogle Scholar
Huang, Y. J. and Prichard, R. K. (1999). Identification and stage specific-specific expression of two putative P-glycoprotein coding genes in Onchocerca volvulus. Molecular and Biochemical Parasitology 102, 273281. doi:10.1016/S0166-6851(99)00104-8.CrossRefGoogle Scholar
Juliano, R. L. and Ling, V. (1976). A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochimica et Biophysica Acta 455, 152162. doi: 10.1016/0005-2736(76)90160-7.CrossRefGoogle ScholarPubMed
Légaré, D., Hettema, E. and Ouellette, M. (1994). The P-glycoprotein-related gene family in Leishmania. Molecular and Biochemical Parasitology 68, 8191. doi:10.1016/0166-6851(94)00156-1.CrossRefGoogle ScholarPubMed
Linton, K. J. and Higgins, C. F. (1998). The Escherichia coli ATP-binding cassette (ABC) proteins. Molecular Microbiology 28, 5–13. doi:10.1046/j.1365-2958.1998.00764.x.CrossRefGoogle ScholarPubMed
Li, B. W., Rush, A. C., Crosby, S. D., Warren, W. C., Williams, S. A., Mitreva, M. and Weil, G. J. (2005). Profiling of gender-regulated gene transcripts in the filarial nematode Brugia malayi by cDNA oligonucleotide array analysis. Molecular and Biochemical Parasitology 143, 4957. doi:10.1016/j.molbiopara.2005.05.005.CrossRefGoogle ScholarPubMed
Liu, C., Oliveira, A., Chauhan, C., Ghedin, E. and Unnasch, T. R. (2010). Functional analysis of putative operons in Brugia malayi. International Journal for Parasitology 40, 6371. doi:10.1016/j.ijpara.2009.07.001.CrossRefGoogle ScholarPubMed
Maser, P. and Kaminsky, R. (1998). Identification of three ABC transporter genes in Trypanosoma brucei spp. Parasitology Research 84, 106111. doi:10.1007/s004360050365.Google ScholarPubMed
Molento, M. B. and Prichard, R. K. (1999). Effects of the multidrug-resistance-reversing agents verapamil and CL 347,099 on the efficacy of ivermectin or moxidectin against unselected and drug-selected strains of Haemonchus contortus in jirds (Meriones unguiculatus). Parasitology Research 85, 10071011. doi:10.1007/s004360050673.CrossRefGoogle ScholarPubMed
Osei-Atweneboana, M. Y., Eng, J. K. L., Boakye, D. A., Gyapong, J. O. and Prichard, R. K. (2007). Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two phase epidemiological study. The Lancet 369, 20212029. doi:10.1016/S0140-6736(07)60942-8.CrossRefGoogle Scholar
Persson, B. and Argos, P. (1994). Prediction of transmembrane segments in proteins utilising multiple sequence alignments. Journal of Molecular Biology 237, 182192. doi:10.1006/jmbi.1994.CrossRefGoogle ScholarPubMed
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.CrossRefGoogle ScholarPubMed
Quentin, Y., Fichant, G. and Denizot, F. (1999). Inventory, assembly and analysis of Bacillus subtilis ABC transport systems. Journal of Molecular Biology 287, 467484. doi:10.1006/jmbi.1999.CrossRefGoogle ScholarPubMed
Schneider, E. and Henke, S. (1998). ATP-binding cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiology Reviews 22, 120.CrossRefGoogle ScholarPubMed
Scott, A. L. and Ghedin, E. (2009). The genome of Brugia malayi – All worms are not created equal. Parasitology International 58, 6–11. doi:10.1016/j.parint.2008.CrossRefGoogle Scholar
Sheps, J. A., Ralph, S., Zhao, Z., Baillie, D. L. and Ling, V. (2004). The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biology 5, R15.CrossRefGoogle ScholarPubMed
Tomii, K. and Kanehisa, M. (1998). A comparative analysis of ABC transporters in complete microbial genomes. Genome Research 8, 10481059. doi:10.1101/gr.8.10.1048.CrossRefGoogle ScholarPubMed
Walker, J. E., Saraste, M., Runswick, M. J. and Gay, N. J. (1982). Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO Journal 1, 945951.CrossRefGoogle Scholar
Wu, C. T., Budding, M., Griffin, M. S. and Croop, J. M. (1991) Isolation and characterization of Drosophila multidrug resistance gene homologs. Molecular Cell Biology 11, 39403948.Google ScholarPubMed
Xu, M., Molento, M., Blackhall, W., Ribeiro, P., Beech, R. and Prichard, R. (1998). Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Molecular and Biochemical Parasitology 91, 327335. doi:10.1016/S0166-6851(97)00215-6.CrossRefGoogle ScholarPubMed
Zhao, Z., Sheps, J. A., Ling, V., Fang, L. L. and Baillie, D. L. (2004). Expression analysis of ABC transporters reveals differential functions of tandemly duplicated genes in Caenorhabditis elegans. Journal of Molecular Biology 344, 409417. doi:10.1016/j.jmb.2004.CrossRefGoogle ScholarPubMed
Zhao, Z., Thomas, J. H., Chen, N., Sheps, J. A. and Baillie, D. L. (2007). Comparative genomics and adaptive selection of the ATP-binding-cassette gene family in Caenorhabditis species. Genetics 175, 14071418. doi:10.1534/genetics.106.066720.CrossRefGoogle ScholarPubMed