Amino acid substitutions of Na,K-ATPase conferring decreased sensitivity to cardenolides in insects compared to mammals

Insect Biochemistry and Molecular Biology - Tập 43 - Trang 1109-1115 - 2013
Safaa Dalla1, Herman G.P. Swarts2, Jan B. Koenderink2, Susanne Dobler1
1Molecular Evolutionary Biology, Biocenter Grindel, Universität Hamburg, Martin-Luther-King Pl. 3, 20146 Hamburg, Germany
2Department of Pharmacology and Toxicology 149, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands

Tài liệu tham khảo

Aardema, 2012, The evolution of cardenolide-resistant forms of Na+, K+-ATPase in Danainae butterflies, Mol. Ecol., 21, 340, 10.1111/j.1365-294X.2011.05379.x Agrawal, 2012, Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions, New Phytol., 194, 28, 10.1111/j.1469-8137.2011.04049.x Al-Robai, 1993, Different ouabain sensitivities of Na+/K+-ATPase from Poekilocerus bufonius tissues and a possible physiological cost, Comp. Biochem. Physiol., 106B, 805 Blanco, 1995, Kinetic properties of the α2β1 and α2β2 isoforms of the Na, K-ATPase, Biochemistry, 34, 319, 10.1021/bi00001a039 Blanco, 1998, Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function, Am. J. Physiol. Ren. Physiol., 275, F633, 10.1152/ajprenal.1998.275.5.F633 Burns, 1993, Random mutagenesis of the sheep Na, K-ATPase alpha 1 subunit generates a novel T797N mutation that results in a ouabain-resistant enzyme, J. Biol. Chem., 268, 25632, 10.1016/S0021-9258(19)74436-6 Croyle, 1997, Extensive random mutagenesis analysis of the Na+/K+-ATPase alpha subunit identifies known and previously unidentified amino acid residues that alter ouabain sensitivity–implications for ouabain binding, Eur. J. Biochem., 248, 488, 10.1111/j.1432-1033.1997.00488.x De Pont, 2009, The non-gastric H, K-ATPase as a tool to study the ouabain-binding site in Na, K-ATPase, Pflugers Arch., 457, 623, 10.1007/s00424-008-0467-8 DeTomaso, 1993, Expression, targeting, and assembly of functional Na, K-ATPase polypeptides in baculovirus-infected insect cells, J. Biol. Chem., 268, 1470, 10.1016/S0021-9258(18)54099-0 Dobler, 2012, Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase, Proc. Natl. Acad. Sci. U.S.A, 109, 13040, 10.1073/pnas.1202111109 Feng, 1994, Analysis of amino acid residues in the H5-H6 transmembrane and extracellular domain of the Na, K-ATPase subunit identified T797 as a determinant of ouabain sensitivity, Biochemistry, 33, 4218, 10.1021/bi00180a015 Hansen, 1984, Interaction of cardiac-glycosides with (Na+ + K+)-activated ATPase – a biochemical link to digitalis-induced inotropy, Pharmacol. Rev., 36, 143 Holzinger, 1992, Molecular basis for the insensitivity of the monarch (Danaus plexippus) to cardiac glycosides, FEBS Lett., 314, 477, 10.1016/0014-5793(92)81530-Y Horisberger, 2004, Recent insights into the stucture and mechanism of the sodium pump, Physiology, 19, 377, 10.1152/physiol.00013.2004 Koenderink, 2000, High-affinity ouabain binding by a chimeric gastric H+, K+-ATPase containing transmembrane hairpins M3–M4 and M5–M6 of the alpha(1)-subunit of rat Na+, K+-ATPase, Proc. Natl. Acad. Sci. U.S.A, 97, 11209, 10.1073/pnas.200109597 Labeyrie, 2004, Molecular adaptation of Chrysochus leaf beetles to toxic compounds in their food plants, Mol. Biol. Evol., 21, 218, 10.1093/molbev/msg240 Laursen, 2013, Crystal structure of the high-affinity Na+, K+-ATPase–ouabain complex with Mg2+ bound in the cation binding site, Proc. Natl. Acad. Sci. U.S.A, 110, 10958, 10.1073/pnas.1222308110 Luckow, 1993, Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli, J. Virol., 67, 4566, 10.1128/JVI.67.8.4566-4579.1993 Malcolm, 1991, Cardenolide-mediated interactions between plants and herbivores, vol. 2, 251 Moore, 1986, Ouabain-resistant Na, K-ATPases and cardenolide tolerance in the large milkweed bug, Oncopeltus fasciatus, J. Insect Physiol., 32, 27, 10.1016/0022-1910(86)90154-X Paula, 2004, Interactions between cardiac glycosides and sodium/potassium-ATPase:  Three-dimensional structure–activity relationship models for ligand binding to the E2-Pi form of the enzyme versus activity inhibition, Biochemistry, 44, 498, 10.1021/bi048680w Petschenka, 2013, Stepwise evolution of resistance to toxic cardenolides via genetic substitutions in the Na+, K+-ATPase of milkweed butterflies (Lepidoptera: Danaini), Evolution, 67, 2753, 10.1111/evo.12152 Price, 1988, Structure-function relationships in the Na, K-ATPase alpha subunit: site-directed mutagenesis of glutamine-111 to arginine and asparagine-122 to aspartic acid generates a ouabain-resistant enzyme, Biochemistry, 27, 8400, 10.1021/bi00422a016 Price, 1990, Structure-function studies of Na, K-ATPase. Site-directed mutagenesis of the border residues from the H1–H2 extracellular domain of the alpha subunit, J. Biol. Chem., 265, 6638, 10.1016/S0021-9258(19)39197-5 Qiu, 2005, Reconstruction of the complete ouabain-binding pocket of Na, K-ATPase in gastric H, K-ATPase by substitution of only seven amino acids, J. Biol. Chem., 280, 32349, 10.1074/jbc.M505168200 Qiu, 2006, Conversion of the low-affinity ouabain-binding site of non-gastric H, K-ATPase into a high-affinity binding site by substitution of only five amino acids, J. Biol. Chem., 281, 13533, 10.1074/jbc.M600551200 Schatzmann, 1953, Herzglycoside als Hemmstoffe für den aktiven Kalium- und Natriumtransport durch die Erythrocytenmembran, Helv. Physiol. Pharmacol. Acta, 11, 346 Skou, 1997, The identification of the sodium pump, Biosci. Rep., 24, 437 Swarts, 2007, The human non-gastric H, K-ATPase has a different cation specificity than the rat enzyme, Biochim. Biophys. Acta, 1768, 580, 10.1016/j.bbamem.2006.10.010 Swarts, 2013, Familial hemiplegic migraine mutations affect Na, K-ATPase domain interactions, Biochim. Biophys. Acta, 1832, 2173, 10.1016/j.bbadis.2013.08.003 Thomas, 1974, Synthesis and biological activity of semisynthetic digitalis analogs, J. Pharm. Sci., 63, 1649, 10.1002/jps.2600631102 Vaughan, 1977, Insensitivity of lepidopteran tissues to ouabain: physiological mechanisms for protection from cardiac glycosides, J. Insect Physiol., 23, 585, 10.1016/0022-1910(77)90052-X Yatime, 2011, Structural insights into the high affinity binding of cardiotonic steroids to the Na+, K+-ATPase, J. Struct. Biol., 174, 296, 10.1016/j.jsb.2010.12.004 Yoda, 1982, Interaction between ouabain and the phosphorylated intermediate of Na, K-ATPase, Mol. Pharmacol., 22, 700 Zhen, 2012, Parallel molecular evolution in an herbivore community, Science, 337, 1634, 10.1126/science.1226630