The ABC transporter gene family of the Pearl oyster (Pinctada fucata)
Abstract
Pearl oyster (Pinctada fucata) is an economically important species cultivated in the South of Thailand. The cultures can be affected by environmental pollution leading to the reduction of growth and survival. Multixenobiotic resistance mechanism has been reported in aquatic organisms mediated by ABC transporters. In bivalves, these proteins have been reported to pump chemical pollutants out of the cells. As a result, those animals can adapt and survive in a polluted environment. However, ABC transporters have not been identified in the Pearl oyster’s genome. We, therefore, investigated the gene family of ABC transporters in this species in order to identify gene numbers and classify them into subfamilies. Also, the evolutionary relationships of this gene family were determined in comparison with other organisms including Drosophila melanogaster, Brachionus koreanus, Caenorhabditis elegans, Saccharomyces cerevisiae and Homo sapiens. In the present study, 65 ABC transporters were identified in the Pearl oyster genome which include 10, 15, 20, 3, 1, 3, 12 and 1 ABC transporters belonging to subfamilies ABCA-ABCH, respectively. Gene expansions were found in subfamilies ABCB, ABCC and ABCG. Members of these subfamilies have been reported to functions as multixenobiotic transporter in aquatic organisms. Therefore multixenobiotic resistance should be exhibited in the Pearl oyster and assist them to adapt and survive in contaminated environments. The results of this work are essential for further investigation of multixenobiotic resistance mechanisms in this species. This would eventually benefit aquaculture practices and would also lead to the study of this gene family functions in other mollusks. Keywords: pearl oyster, phylogenetic tree, ABC transporter, gene, proteinReferences
Alaimo, C., Catrein, I., Morf, L., Marolda, C.L., Callewaert, N., Valvano, M.A., Feldman, M.F. & Aebi, M. (2006). Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. The EMBO Journal, 25(5), 967-976.
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402.
Andersen, D.S., & Leevers, S.J. (2007). The essential Drosophila ATP-binding cassette domain protein, pixie, binds the 40 S ribosome in an ATP-dependent manner and is required for translation initiation. Journal of Biological Chemistry, 282(20), 14752-14760.
Annilo, T., Chen, Z.Q., Shulenin, S., Costantino, J., Thomas, L., Lou, H., Stefanov, S. & Dean, M. (2006). Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics, 88(1), 1-11.
Barthelme, D., Dinkelaker, S., Albers, S.V., Londei, P., Ermler, U., & Tampé, R. (2011). Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. Proceedings of the National Academy of Sciences, 108(8), 3228-3233.
Birney, E., Clamp, M., & Durbin, R. (2004). GeneWise and genomewise. Genome Research, 14(5), 988-995.
Bisbal, C., Martinand, C., Silhol, M., Lebleu, B., & Salehzada, T. (1995). Cloning and characterization of a RNase L inhibitor. A new component of the interferon-regulated 2-5 A pathway. Biol. Chem, 270, 13308-13317.
Broehan, G., Kroeger, T., Lorenzen, M., & Merzendorfer, H. (2013). Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics 14, 6.
Cai, S.Y., Soroka, C.J., Ballatori, N., & Boyer, J.L. (2003). Molecular characterization of a multidrug resistance-associated protein, Mrp2, from the little skate. Am J Physiol Regul Integr Comp Physiol, 284,
R125–R130.
Cole, S.P., & Deeley, R.G. (2006). Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol. Sci, 27, 438-446.
Dawson, R.J., & Locher, K.P. (2006). Structure of a bacterial multidrug ABC transporter. Nature, 443(7108), 180.
Dean, M., Hamon, Y., & Chimini, G. (2001). The human ATP-binding cassette (ABC) transporter superfamily. Journal of Lipid Research, 42, 1007–17.
Decottignies, A., & Goffeau, A. (1997). Complete inventory of the yeast ABC proteins. Nat Genet, 15, 137-145.
Deeley, R.G., Westlake, C., & Cole, S. (2006). Transmembrane transport of endo- and xenobiotics by the ATP binding cassette multidrug resistance proteins (MRP). Physiol Rev, 86, 849-899.
Dermauw, W., & Van Leeuwen, T. (2014). The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochemistry and Molecular Biology, 45, 89-110.
Grbić, M., Van Leeuwen, T., Clark, R.M., Rombauts, S., Rouzé, P., Grbić, V., Osborne, E.J., Dermauw, W., Ngoc, P.C.T., Ortego, F., Hernández-Crespo, P., Diaz, I., Martinez, M., Navajas, M., Sucena, E., Magalhães, S., Nagy, L., Pace, R. M., Djuranović, S., Smagghe, G., Iga, M., Christiaens, O., Veenstra, J. A., Ewer, J., Villalobos R. M., Hutter J. L., Hudson, S. D., Velez, M., Yi, S. V., Zeng, J., Pires-daSilva, A., Roch, F., Cazaux, M., Navarro, M., Zhurov, V., Acevedo, G., Bjelica, A., Fawcett, J. A., Bonnet, E., Martens, C., Baele, G., Wissler, L., Sanchez-Rodriguez, A., Tirry, L., Blais, C., Demeestere, K., Henz, S. R., Gregory, T. R., Mathieu, J., Verdon, L., Farinelli, L., Schmutz, J., Lindquist, E., Feyereisen, R., & Van de Peer, Y. (2011). The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374), 487.
Gottesman, M.M., Fojo, T., & Bates, S.E. (2002). Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer, 2, 48-58.
Hassel, B.A., Zhou, A., Sotomayor, C., Maran, A., & Silverman, R.H. (1993). A dominant negative mutant of 2-5A-dependent RNase suppresses antiproliferative and antiviral effects of interferon. EMBO J, 12, 3297-3304.
Higgins, C. F. (1992). ABC transporters: from microorganisms to man. Annual Review of Cell Biology, 8(1), 67-113.
Higgins, E.T. (1998). Promotion and prevention: Regulatory focus as a motivational principle. In Advances in Experimental Social Psychology (Vol. 30, pp. 1-46). Academic Press.
Higgins, C.F., & Linton, K.J. (2004). The ATP switch model for ABC transporters. Nature Structural and Molecular Biology, 11(10), 918.
Higgins, C.F. (2007). Multiple molecular mechanisms for multidrug resistance transporters. Nature, 446(7137), 749.
Jeong, C.B., Kim, B.M., Lee, J.S., & Rhee, J.S. (2014). Genome-wide identification of whole ATP-binding cassette (ABC) transporters in the intertidal copepod Tigriopus japonicus. BMC Genomics, 15(1), 651.
Jeong, C.B., Kim, H.S., Kang, H.M., Lee, Y.H., Zhou, B., Choe, J., & Lee, J.S. (2017). Genome-wide identification of ATP-binding cassette (ABC) transporters and conservation of their xenobiotic transporter function in the monogonont rotifer (Brachionus koreanus). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 21, 17-26.
Jones, P., Binns, D., Chang, H.Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., Pesseat, S., Quinn, A. F., Sangrador-Vegas, A., Scheremetjew, M. Yong, S. Y., Lopez, R., & Hunter, S. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics, 30(9), 1236-1240.
Kanjanachatree, K., Piyathamrongrut, K., & Rativat, V. (2004). The culture of pearl oysters, Pinctada fucata (Gould, 1850) in Phuket with temperature shock method and survival rates on various feeds. Songklanakarin J. Sci. Technol, 27, 1-16.
Katoh, K., & Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780.
Kingtong, S., Chitramvong, Y., & Janvilisri, T. (2007). ATP-binding cassette multidrug transporters in Indian-rock oyster Saccostrea forskali and their role in the export of an environmental organic pollutant tributyltin. Aquatic Toxicology, 85(2), 124-132.
Kurelec, B. (1992). The multixenobiotic resistance mechanism in aquatic organisms. Crit Rev Toxicol, 22,
23–43.
Leslie, E.M. (2012). Arsenice-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). Inorg Biochem, 108, 141-149.
Luedeking, A., & Koehler, A. (2004). Regulation of expression of multixenobiotic (MXR) genes by environmental factors in the blue mussel Mytilus edulis. Aquat Toxicol, 69, 1–10.
McFadzen, I., Eufemia, N., Heath, C., Epel, D., Moore, M.N., & Lowe, D. (2000). Multidrug resistance in the embryos and larvae of the mussel Mytilus edulis. Mar Environ Res, 50, 319–323.
Miller, D.S., Graeff, C., Droulle, L., Fricker, S., & Fricker, G. (2002). Xenobiotic efflux pumps in isolated fish brain capillaries. Am J Physiol Regul Integr Comp Physiol, 282, R191–R198.
Minier, C., & Moore, M.N. (1996). Rhodamine B accumulation and MXR protein expression in mussel blood cells: effects of exposure to vincristine. Mar Ecol Prog Ser, 142, 165–173.
Paytubi, S., Wang, X., Lam, Y.W., Izquierdo, L., Hunter, M.J., Jan, E., Hundal, H.S., & Proud, C.G. (2009). ABC50 promotes translation initiation in mammalian cells. Journal of Biological Chemistry, 284(36), 24061-24073.
Rees, D.C., Johnson, E., & Lewinson, O. (2009). ABC transporters: the power to change. Nature Reviews Molecular Cell Biology, 10(3), 218.
Reese, M.G., Eeckman, F.H., Kulp, D., & Haussler, D. (1997). Improved splice site detection in Genie. Journal of Computational Biology, 4(3), 311-323.
Rioult, D., Pasquier, J., Boulangé-Lecomte, C., Poret, A., Abbas, I., Marin, M., Minier C., & Le Foll, F. (2014). The multi-xenobiotic resistance (MXR) efflux activity in hemocytes of Mytilus edulis is mediated by an ATP binding cassette transporter of class C (ABCC) principally inducible in eosinophilic granulocytes. Aquatic Toxicology. 153, 98-109.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.
Sauerborn, R., Polancec, D.S., Zaja, R., & Smital, T. (2004). Identification of the multidrug resistance-associated protein (mrp) related gene in red mullet (Mullus barbatus). Mar Environ Res, 58,
199–204.
Sheps, J.A., Ralph, S., Zhao, Z., Baillie, D.L., & 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(3), R15.
Smital, T., Sauerborn, R., & Hackenberger, B.K. (2003). Inducibility of the P-glycoprotein transport activity in the marine mussel Mytilus galloprovincialis and the freshwater mussel Dreissena polymorpha. Aquatic Toxicology, 65(4), 443-465.
Sturm, A., Cunningham, P., & Dean, M. (2009). The ABC transporter gene family of Daphnia pulex. BMC Genomics, 10(1), 170.
Takeuchi, T., Kawashima, T., Koyanagi, R., Gyoja, F., Tanaka, M., Ikuta, T., Shoguchi, E., Fujiwara, M., Shinzato, C., Hisata, K. & Fujie, M. (2012). Draft genome of the pearl oyster Pinctada fucata: a platform for understanding bivalve biology. DNA Research, 19(2), 117-130.
Takeuchi, T., Koyanagi, R., Gyoja, F., Kanda, M., Hisata, K., Fujie, M., Goto, H., Yamasaki, S., Nagai, K., Morino, Y. & Miyamoto, H. (2016). Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle. Zoological Letters, 2(1), 3.
Vasiliou, V., Vasiliou, K., & Nebert, D.W. (2009). Human ATP-binding cassette (ABC) transporter family. Hum Genomics, 3(3), 281-290.
Wu, B., Torres-Duarte, C., Cole, B.J., & Cherr, G.N. (2015). Copper oxide and zinc oxide nanomaterials act as inhibitors of multidrug resistance transport in sea urchin embryos: their role as chemosensitizers. Environmental Science & Technology, 49(9), 5760-5770.
Wenzel, S., Wilbraham, D., Fuller, R., Getz, E.B., & Longphre, M. (2007). Effect of an interleukin-4 variant on late phase asthmatic response to allergen challenge in asthmatic patients: results of two phase 2a studies. The Lancet, 370(9596), 1422-1431.
Zaja, R., Klobucar, R.S., & Smital, T. (2007). Detection and functional characterization of Pgp1 (ABCB1) and MRP3 (ABCC3) efflux transporters in the PLHC-1 fish hepatoma cell line. Aquat Toxicol, 81, 365–376
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402.
Andersen, D.S., & Leevers, S.J. (2007). The essential Drosophila ATP-binding cassette domain protein, pixie, binds the 40 S ribosome in an ATP-dependent manner and is required for translation initiation. Journal of Biological Chemistry, 282(20), 14752-14760.
Annilo, T., Chen, Z.Q., Shulenin, S., Costantino, J., Thomas, L., Lou, H., Stefanov, S. & Dean, M. (2006). Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics, 88(1), 1-11.
Barthelme, D., Dinkelaker, S., Albers, S.V., Londei, P., Ermler, U., & Tampé, R. (2011). Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. Proceedings of the National Academy of Sciences, 108(8), 3228-3233.
Birney, E., Clamp, M., & Durbin, R. (2004). GeneWise and genomewise. Genome Research, 14(5), 988-995.
Bisbal, C., Martinand, C., Silhol, M., Lebleu, B., & Salehzada, T. (1995). Cloning and characterization of a RNase L inhibitor. A new component of the interferon-regulated 2-5 A pathway. Biol. Chem, 270, 13308-13317.
Broehan, G., Kroeger, T., Lorenzen, M., & Merzendorfer, H. (2013). Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics 14, 6.
Cai, S.Y., Soroka, C.J., Ballatori, N., & Boyer, J.L. (2003). Molecular characterization of a multidrug resistance-associated protein, Mrp2, from the little skate. Am J Physiol Regul Integr Comp Physiol, 284,
R125–R130.
Cole, S.P., & Deeley, R.G. (2006). Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol. Sci, 27, 438-446.
Dawson, R.J., & Locher, K.P. (2006). Structure of a bacterial multidrug ABC transporter. Nature, 443(7108), 180.
Dean, M., Hamon, Y., & Chimini, G. (2001). The human ATP-binding cassette (ABC) transporter superfamily. Journal of Lipid Research, 42, 1007–17.
Decottignies, A., & Goffeau, A. (1997). Complete inventory of the yeast ABC proteins. Nat Genet, 15, 137-145.
Deeley, R.G., Westlake, C., & Cole, S. (2006). Transmembrane transport of endo- and xenobiotics by the ATP binding cassette multidrug resistance proteins (MRP). Physiol Rev, 86, 849-899.
Dermauw, W., & Van Leeuwen, T. (2014). The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochemistry and Molecular Biology, 45, 89-110.
Grbić, M., Van Leeuwen, T., Clark, R.M., Rombauts, S., Rouzé, P., Grbić, V., Osborne, E.J., Dermauw, W., Ngoc, P.C.T., Ortego, F., Hernández-Crespo, P., Diaz, I., Martinez, M., Navajas, M., Sucena, E., Magalhães, S., Nagy, L., Pace, R. M., Djuranović, S., Smagghe, G., Iga, M., Christiaens, O., Veenstra, J. A., Ewer, J., Villalobos R. M., Hutter J. L., Hudson, S. D., Velez, M., Yi, S. V., Zeng, J., Pires-daSilva, A., Roch, F., Cazaux, M., Navarro, M., Zhurov, V., Acevedo, G., Bjelica, A., Fawcett, J. A., Bonnet, E., Martens, C., Baele, G., Wissler, L., Sanchez-Rodriguez, A., Tirry, L., Blais, C., Demeestere, K., Henz, S. R., Gregory, T. R., Mathieu, J., Verdon, L., Farinelli, L., Schmutz, J., Lindquist, E., Feyereisen, R., & Van de Peer, Y. (2011). The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374), 487.
Gottesman, M.M., Fojo, T., & Bates, S.E. (2002). Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer, 2, 48-58.
Hassel, B.A., Zhou, A., Sotomayor, C., Maran, A., & Silverman, R.H. (1993). A dominant negative mutant of 2-5A-dependent RNase suppresses antiproliferative and antiviral effects of interferon. EMBO J, 12, 3297-3304.
Higgins, C. F. (1992). ABC transporters: from microorganisms to man. Annual Review of Cell Biology, 8(1), 67-113.
Higgins, E.T. (1998). Promotion and prevention: Regulatory focus as a motivational principle. In Advances in Experimental Social Psychology (Vol. 30, pp. 1-46). Academic Press.
Higgins, C.F., & Linton, K.J. (2004). The ATP switch model for ABC transporters. Nature Structural and Molecular Biology, 11(10), 918.
Higgins, C.F. (2007). Multiple molecular mechanisms for multidrug resistance transporters. Nature, 446(7137), 749.
Jeong, C.B., Kim, B.M., Lee, J.S., & Rhee, J.S. (2014). Genome-wide identification of whole ATP-binding cassette (ABC) transporters in the intertidal copepod Tigriopus japonicus. BMC Genomics, 15(1), 651.
Jeong, C.B., Kim, H.S., Kang, H.M., Lee, Y.H., Zhou, B., Choe, J., & Lee, J.S. (2017). Genome-wide identification of ATP-binding cassette (ABC) transporters and conservation of their xenobiotic transporter function in the monogonont rotifer (Brachionus koreanus). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 21, 17-26.
Jones, P., Binns, D., Chang, H.Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., Pesseat, S., Quinn, A. F., Sangrador-Vegas, A., Scheremetjew, M. Yong, S. Y., Lopez, R., & Hunter, S. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics, 30(9), 1236-1240.
Kanjanachatree, K., Piyathamrongrut, K., & Rativat, V. (2004). The culture of pearl oysters, Pinctada fucata (Gould, 1850) in Phuket with temperature shock method and survival rates on various feeds. Songklanakarin J. Sci. Technol, 27, 1-16.
Katoh, K., & Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780.
Kingtong, S., Chitramvong, Y., & Janvilisri, T. (2007). ATP-binding cassette multidrug transporters in Indian-rock oyster Saccostrea forskali and their role in the export of an environmental organic pollutant tributyltin. Aquatic Toxicology, 85(2), 124-132.
Kurelec, B. (1992). The multixenobiotic resistance mechanism in aquatic organisms. Crit Rev Toxicol, 22,
23–43.
Leslie, E.M. (2012). Arsenice-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). Inorg Biochem, 108, 141-149.
Luedeking, A., & Koehler, A. (2004). Regulation of expression of multixenobiotic (MXR) genes by environmental factors in the blue mussel Mytilus edulis. Aquat Toxicol, 69, 1–10.
McFadzen, I., Eufemia, N., Heath, C., Epel, D., Moore, M.N., & Lowe, D. (2000). Multidrug resistance in the embryos and larvae of the mussel Mytilus edulis. Mar Environ Res, 50, 319–323.
Miller, D.S., Graeff, C., Droulle, L., Fricker, S., & Fricker, G. (2002). Xenobiotic efflux pumps in isolated fish brain capillaries. Am J Physiol Regul Integr Comp Physiol, 282, R191–R198.
Minier, C., & Moore, M.N. (1996). Rhodamine B accumulation and MXR protein expression in mussel blood cells: effects of exposure to vincristine. Mar Ecol Prog Ser, 142, 165–173.
Paytubi, S., Wang, X., Lam, Y.W., Izquierdo, L., Hunter, M.J., Jan, E., Hundal, H.S., & Proud, C.G. (2009). ABC50 promotes translation initiation in mammalian cells. Journal of Biological Chemistry, 284(36), 24061-24073.
Rees, D.C., Johnson, E., & Lewinson, O. (2009). ABC transporters: the power to change. Nature Reviews Molecular Cell Biology, 10(3), 218.
Reese, M.G., Eeckman, F.H., Kulp, D., & Haussler, D. (1997). Improved splice site detection in Genie. Journal of Computational Biology, 4(3), 311-323.
Rioult, D., Pasquier, J., Boulangé-Lecomte, C., Poret, A., Abbas, I., Marin, M., Minier C., & Le Foll, F. (2014). The multi-xenobiotic resistance (MXR) efflux activity in hemocytes of Mytilus edulis is mediated by an ATP binding cassette transporter of class C (ABCC) principally inducible in eosinophilic granulocytes. Aquatic Toxicology. 153, 98-109.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.
Sauerborn, R., Polancec, D.S., Zaja, R., & Smital, T. (2004). Identification of the multidrug resistance-associated protein (mrp) related gene in red mullet (Mullus barbatus). Mar Environ Res, 58,
199–204.
Sheps, J.A., Ralph, S., Zhao, Z., Baillie, D.L., & 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(3), R15.
Smital, T., Sauerborn, R., & Hackenberger, B.K. (2003). Inducibility of the P-glycoprotein transport activity in the marine mussel Mytilus galloprovincialis and the freshwater mussel Dreissena polymorpha. Aquatic Toxicology, 65(4), 443-465.
Sturm, A., Cunningham, P., & Dean, M. (2009). The ABC transporter gene family of Daphnia pulex. BMC Genomics, 10(1), 170.
Takeuchi, T., Kawashima, T., Koyanagi, R., Gyoja, F., Tanaka, M., Ikuta, T., Shoguchi, E., Fujiwara, M., Shinzato, C., Hisata, K. & Fujie, M. (2012). Draft genome of the pearl oyster Pinctada fucata: a platform for understanding bivalve biology. DNA Research, 19(2), 117-130.
Takeuchi, T., Koyanagi, R., Gyoja, F., Kanda, M., Hisata, K., Fujie, M., Goto, H., Yamasaki, S., Nagai, K., Morino, Y. & Miyamoto, H. (2016). Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle. Zoological Letters, 2(1), 3.
Vasiliou, V., Vasiliou, K., & Nebert, D.W. (2009). Human ATP-binding cassette (ABC) transporter family. Hum Genomics, 3(3), 281-290.
Wu, B., Torres-Duarte, C., Cole, B.J., & Cherr, G.N. (2015). Copper oxide and zinc oxide nanomaterials act as inhibitors of multidrug resistance transport in sea urchin embryos: their role as chemosensitizers. Environmental Science & Technology, 49(9), 5760-5770.
Wenzel, S., Wilbraham, D., Fuller, R., Getz, E.B., & Longphre, M. (2007). Effect of an interleukin-4 variant on late phase asthmatic response to allergen challenge in asthmatic patients: results of two phase 2a studies. The Lancet, 370(9596), 1422-1431.
Zaja, R., Klobucar, R.S., & Smital, T. (2007). Detection and functional characterization of Pgp1 (ABCB1) and MRP3 (ABCC3) efflux transporters in the PLHC-1 fish hepatoma cell line. Aquat Toxicol, 81, 365–376
Downloads
Published
2018-09-17
Issue
Section
Research Article
