Functional evidence for physiological mechanisms to circumvent neurotoxicity of cardenolides in an adapted and a non-adapted hawk-moth species

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1759, 2013, Pages

  Petschenka, Georg ^a   Pick, Christian ^a   Wagschal, Vera ^a   Dobler, Susanne ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Cardenolides; Daphnis nerii; Manduca sexta; P glycoprotein; Resistance

Indexed keywords

ADAPTATION; CATION; FEEDING; FUNCTIONAL ROLE; GENE EXPRESSION; INHIBITION; INHIBITOR; MOTH; NEUROLOGY; PHYSIOLOGY; PROTEIN; STEROID;

EID: 84875334427     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.3089     Document Type: Article

References (45)

1. Scudder GGE, Meredith J. 1982 The permeability of the midgut of three insects to cardiac glycosides. J. Insect Physiol. 28, 689-694. (doi:10.1016/0022-1910(82)90147-0)
2. Despres L, David JP, Gallet C. 2007 The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298-307. (doi:10.1016/j.tree. 2007.02.010)
3. Luckner M, Wichtl M. 2000 Digitalis. Stuttgart, Germany: Wissenschaftliche Verlagsgesellschaft mbH.
4. Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S. 2012 Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol. 194, 28-45. (doi:10.1111/j.1469-8137.2011.04049.x)
5. Schatzmann H-J. 1953 Herzglykoside als Hemmstoffe für den aktiven Kalium-und Natriumtransport durch die Erythrocytenmembran. Helv. Physiol. Pharmacol. Acta 11, 346-354.
6. Horisberger JD. 2004 Recent insights into the structure and mechanism of the sodium pump. Physiology 19, 377-387. (doi:10.1152/physiol. 00013.2004)
7. Brower LP, Van Zandt Brower J, Corvino JM. 1967 Plant poisons in a terrestrial food chain. Proc. Natl Acad. Sci. USA 57, 893-898. (doi:10.1073/pnas.57.4.893)
8. Vaughan GL, Jungreis AM. 1977 Insensitivity of lepidopteran tissues to ouabain: physiological mechanisms for protection from cardiac glycosides. J. Insect Physiol. 23, 585-589. (doi:10.1016/0022-1910(77)90052-X)
9. +-ATPase. J. Chem. Ecol. 22, 1921-1937. (doi:10. 1007/BF02028512)
10. +-ATPase of the oleander hawk moth (Daphnis nerii) is highly susceptible to cardenolides. Chemoecology 19, 235-239. (doi:10.1007/s00049-009-0025-7)
11. +-ATPase in cardenolideadapted Lepidoptera. J. Insect Physiol. 58, 607-612. (doi:10.1016/j.jinsphys.2011.12.012)
12. +-ATPase in milkweed butterflies. Chemoecology 10, 201-203. (doi:10.1007/PL00001823)
13. Mebs D, Reuss E, Schneider M. 2005 Studies on the cardenolide sequestration in African milkweed butterflies (Danaidae). Toxicon 45, 581-584. (doi:10.1016/j.toxicon.2004.12.017)
14. Pichon Y, Sattelle DB, Lane NJ. 1972 Conduction processes in the nerve cord of the moth Manduca sexta in relation to its ultrastructure and haemolymph ionic composition. J. Exp. Biol. 56, 717-734.
15. Murray CL, Quaglia M, Arnason JT, Morris CE. 1994 A putative nicotine pump at the metabolic blood-brain barrier of the tobacco hornworm. J. Neurobiol. 25, 23-34. (doi:10.1002/neu.480250103)
16. Abe F, Yamauchi T, Minato K. 1996 Presence of cardenolides and ursolic acid from oleander leaves in larvae and frass of Daphnis nerii. Phytochemistry 42, 45-49. (doi:10.1016/0031-9422(95)00837-3)
17. Rubin AL, Stirling CE, Stahl WL. 1983 3H-ouabain binding autoradiography in the abdominal nerve cord of the hawk moth, Manduca sexta. J. Exp. Biol. 104, 217-230.
18. Petropoulos S, Gibb W, Matthews SG. 2010 Effect of glucocorticoids on regulation of placental multidrug resistance phosphoglycoprotein (P-gp) in the mouse. Placenta 31, 803-810. (doi:10.1016/j. placenta.2010.06.014)
19. de Boer AG, van der Sandt ICJ, Gaillard PJ. 2003 The role of drug transporters at the blood-brain barrier. Annu. Rev. Pharmacol. Toxicol. 43, 629-656. (doi:10. 1146/annurev.pharmtox.43.100901.140204)
20. Tanigawara Y, Okamura N, Hirai M, Yasuhara M, Ueda K, Kioka N, Komano T, Hori R. 1992 Transport of digoxin by human P-glycoprotein expressed in a porcine kidney epithelial cell line (LLC-PK1). J. Pharmacol. Exp. Ther. 263, 840-845.
21. Lanning CL, Fine RL, Corcoran JJ, Ayad HM, Rose RL, Abou-Donia MB. 1996 Tobacco budworm Pglycoprotein: biochemical characterization and its involvement in pesticide resistance. Biochim. Biophys. Acta 1291, 155-162. (doi:10.1016/0304-4165(96)00060-8)
22. Podsiadlowski L, Matha V, Vilcinskas A. 1998 Detection of a P-glycoprotein related pump in Chironomus larvae and its inhibition by verapamil and cyclosporin A. Comp. Biochem. Phys. B 121, 443-450. (doi:10.1016/S0305-0491(98)10137-2)
23. Johnston RM, Levine RB. 1996 Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta. J. Neurophysiol. 76, 3178-3195.
24. Woods A, Chamberlin ME. 1999 Effects of dietary protein concentration on L-proline transport by Manduca sexta midgut. J. Insect Physiol. 45, 735-741. (doi:10.1016/s0022-1910(99)00050-5)
25. 3H]vinblastine transport by isolated vesicles. Biochim. Biophys. Acta 1061, 106-110. (doi:10.1016/0005-2736(91)90274-C)
26. Yasuhara JC, Baumann O, Takeyasu K. 2000 Localization of Na/K-ATPase in developing and adult Drosophila melanogaster photoreceptors. Cell Tissue Res. 300, 239-249. (doi:10.1007/s004410000195)
27. +-ATPase expression patterns in the osmoregulatory organs of larval and adult mosquito Aedes aegypti. J. Exp. Biol. 209, 4638-4651. (doi:10.1242/jeb.02551)
28. Labbé R, Caveney S, Donly C. 2011 Genetic analysis of the xenobiotic resistance-associated ABC gene subfamilies of the Lepidoptera. Insect Mol. Biol. 20, 243-256. (doi:10.1111/j.1365-2583.2010.01064.x)
29. Wu CT, Budding M, Griffin MS, Croop JM. 1991 Isolation and characterization of Drosophila multidrug resistance gene homologs. Mol. Cell. Biol. 11, 3940-3948.
30. Gerrard B, Stewart C, Dean M. 1993 Analysis of Mdr50: a Drosophila P-glycoprotein/multidrug resistance gene homolog. Genomics 17, 83-88. (doi:10.1006/geno.1993.1286)
31. Katoh K, Kuma K-i, Toh H, Miyata T. 2005 MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518. (doi:10.1093/nar/gki198)
32. Castresana J. 2000 Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552. (doi:10.1093/oxfordjournals.molbev.a026334)
33. Huelsenbeck JP, Ronquist F. 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. (doi:10.1093/bioinformatics/17.8.754)
34. Whelan S, Goldman N. 2001 A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699. (doi:10. 1093/oxfordjournals.molbev.a003851)
35. van den Elsen JMH, Kuntz DA, Hoedemaeker FJ, Rose DR. 1999 Antibody C219 recognizes an a-helical epitope on P-glycoprotein. Proc. Natl Acad. Sci. USA 96, 13 679-13 684.
36. Moore LV, Scudder GGE. 1986 Ouabain-resistant Na, K-ATPases and cardenolide tolerance in the large milkweed bug, Oncopeltus fasciatus. J. Insect Physiol. 32, 27-33. (doi:10.1016/0022-1910(86)90154-X)
37. +activated ATPase to fluid production by malpighian tubules of Locusta migratoria. J. Insect Physiol. 21, 1779-1784. (doi:10.1016/0022-1910(75)90240-1)
38. +)-activated ATPase in the rectal epithelium of the american cockroach, Periplaneta americana. Insect Biochem. 6, 513-517. (doi:10.1016/0020-1790(76)90077-9)
39. +-activated ATPase in the hindgut of two insects Schistocerca and Blaberus. Insect Biochem. 7, 393-395. (doi:10. 1016/0020-1790(77)90043-9)
40. Mayer U, Wagenaar E, Beijnen JH, Smit JW, Meijer DK, van Asperen J, Borst P, Schinkel AH. 1996 Substantial excretion of digoxin via the intestinal mucosa and prevention of long-term digoxin accumulation in the brain by the mdr 1a P-glycoprotein. Br. J. Pharmacol. 119, 1038-1044. (doi:10.1111/j.1476-5381.1996.tb15775.x)
41. Tapadia MG, Lakhotia SC. 2005 Expression of mdr49 and mdr65 multidrug resistance genes in larval tissues of Drosophila melanogaster under normal and stress conditions. Cell Stress Chaperon 10, 7-11. (doi:10.1379/CSC-67R.1)
42. Maddrell S, Gardiner B. 1976 Excretion of alkaloids by malpighian tubules of insects. J. Exp. Biol. 64, 267-281.
43. Gaertner L, Murray C, Morris C. 1998 Transepithelial transport of nicotine and vinblastine in isolated malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism. J. Exp. Biol. 201, 2637-2645.
44. Seiber JN, Tuskes PM, Brower LP, Nelson CJ. 1980 Pharmacodynamics of some individual milkweed cardenolides fed to larvae of the monarch butterfly (Danaus plexippus L.). J. Chem. Ecol. 6, 321-339. (doi:10.1007/BF01402911)
45. Yao HM, Chiou WL. 2006 The complexity of intestinal absorption and exsorption of digoxin in rats. Int. J. Pharm. 322, 79-86. (doi:10.1016/j. ijpharm.2006.05.030)