The ABC gene family in arthropods: Comparative genomics and role ininsecticide transport and resistance

Insect Biochemistry and Molecular Biology

Volumn 45, Issue 1, 2014, Pages 89-110

  Dermauw, Wannes ^a   Van Leeuwen, Thomas ^a,b  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Allelochemicals; Arthropoda; BCRP; Bt toxins; Detoxification; MDR; MRP; Multidrug resistance; P gp; Phase III; Primary carriers; SUR; Traffic ATPases

Indexed keywords

ABC TRANSPORTER; BREAST CANCER RESISTANCE PROTEIN;

ALLELOCHEMICALS; ANIMAL; ARTHROPOD; BT TOXINS; CHEMICAL STRUCTURE; CHEMISTRY; DETOXIFICATION; DROSOPHILA; GENETICS; GENOMICS; INSECTICIDE RESISTANCE; MDR; METABOLISM; MRP; MULTIDRUG RESISTANCE; P-GP; PHASE III; PHYLOGENY; PHYSIOLOGY; PRIMARY CARRIERS; REVIEW; SUR; TRAFFIC ATPASES;

ALLELOCHEMICALS; ARTHROPODA; BCRP; BT TOXINS; DETOXIFICATION; MDR; MRP; MULTIDRUG RESISTANCE; P-GP; PHASE III; PRIMARY CARRIERS; SUR; TRAFFIC ATPASES;

ANIMALS; ARTHROPODS; ATP-BINDING CASSETTE TRANSPORTERS; DROSOPHILA; GENOMICS; INSECTICIDE RESISTANCE; MODELS, MOLECULAR; PHYLOGENY;

EID: 84891764754     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2013.11.001     Document Type: Review

References (194)

1. Akiyama M. The roles of ABCA12 in epidermal lipid barrier formation and keratinocyte differentiation. Biochim. Biophys. Acta 2013, 10.1016/j.bbalip.2013.08.009.
2. Akrouh A., Halcomb S.E., Nichols C.G., Sala-Rabanal M. Molecular biology of K-ATP channels and implications for health and disease. IUBMB Life 2009, 61:971-978.
3. Andersen D.S., Leevers S.J. 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. J.Biol. Chem. 2007, 282:14752-14760.
4. Ardelli B.F. Transport proteins of the ABC systems superfamily and their role in drug action and resistance in nematodes. Parasitol. Int. 2013, 62:639-646.
5. Atsumi S., Miyamoto K., Yamamoto K., Narukawa J., Kawai S., Sezutsu H., Kobayashi I., Uchino K., Tamura T., Mita K., Kadono-Okuda K., Wada S., Kanda K., Goldsmith M.R., Noda H. Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E1591-E1598.
6. Aurade R., Jayalakshmi S.K., Sreeramulu K. Stimulatory effect of insecticides on partially purified P-glycoprotein ATPase from the resistant pest Helicoverpa armigera. Biochem. Cell Biol. 2006, 84:1045-1050.
7. Aurade R., Jayalakshmi S., Sreeramulu K. Modulatory effects of natural curcuminoids on P-glycoprotein ATPase of insecticide-resistant pest Helicoverpa armigera (Lepidopetera: Noctüidae). J.Membr. Biol. 2010, 236:271-278.
8. Aurade R.M., Jayalakshmi S.K., Sreeramulu K. P-glycoprotein ATPase from the resistant pest, Helicoverpa armigera: purification, characterization and effect of various insecticides on its transport function. Biochim. Biophys. Acta 2010, 1798:1135-1143.
9. Aurade R.M., Akbar S.M., Goud H., Jayalakshmi S.K., Sreeramulu K. Inhibition of P-glycoprotein ATPase and its transport function of Helicoverpa armigera by morin, quercetin and phloroglucinol. Pestic. Biochem. Physiol. 2011, 101:212-219.
10. Aurade R.M., Jayalakshmi S.K., Udikeri S.S., Sreeramulu K. Modulation of P-glycoprotein ATPase of Helicoverpa armigera by cholesterol: effects on ATPase activity and interaction of insecticides. Arch. Insect Biochem. Physiol. 2012, 79:47-60.
11. Ballatori N., Krance S.M., Marchan R., Hammond C.L. Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology. Mol. Asp. Med. 2009, 30:13-28.
12. Bao Y.-Y., Li B.-L., Liu Z.-B., Xue J., Zhu Z.-R., Cheng J.-A., Zhang C.-X. Triazophos up-regulated gene expression in the female brown planthopper, Nilaparvata lugens. J.Insect Physiol. 2010, 56:1087-1094.
13. Bariami V., Jones C.M., Poupardin R., Vontas J., Ranson H. Gene amplification, ABC transporters and cytochrome P450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLoS Negl. Trop. Dis. 2012, 6:e1692.
14. Barthelme D., Dinkelaker S., Albers S.-V., Londei P., Ermler U., Tampe R. Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3228-3233.
15. Baxter S.W., Badenes-Perez F.R., Morrison A., Vogel H., Crickmore N., Kain W., Wang P., Heckel D.G., Jiggins C.D. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 2011, 189:U675-U814.
16. Beckstead R.B., Lam G., Thummel C.S. Specific transcriptional responses to juvenile hormone and ecdysone in Drosophila. Insect Biochem. Mol. Biol. 2007, 37:570-578.
17. Begun D.J., Whitley P. Genetics of α-amanitin resistance in a natural population of Drosophila melanogaster. Heredity 2000, 85:184-190.
18. Blattner F.R., Plunkett G., Bloch C.A., Perna N.T., Burland V., Riley M., ColladoVides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453.
19. Bonizzoni M., Afrane Y., Dunn W.A., Atieli F.K., Zhou G., Zhong D., Li J., Githeko A., Yan G. Comparative transcriptome analyses of deltamethrin-resistant and -susceptible Anopheles gambiae mosquitoes from Kenya by RNA-Seq. PLoS ONE 2012, 7:e44607.
20. Borycz J., Borycz J.A., Kubow A., Lloyd V., Meinertzhagen I.A. Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. J.Exp. Biol. 2008, 211:3454-3466.
21. Bravo A., Likitvivatanavong S., Gill S.S., Soberón M. Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 2011, 41:423-431.
22. Broehan G., Kroeger T., Lorenzen M., Merzendorfer H. Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics 2013, 14.
23. Bryon A., Wybouw N., Dermauw W., Tirry L., Van Leeuwen T. Genome wide gene-expression analysis of facultative reproductive diapause in the two-spotted spider mite Tetranychus urticae. BMC Genomics 2013, 14:815.
24. Buchmann J., Meyer C., Neschen S., Augustin R., Schmolz K., Kluge R., Al-Hasani H., Jürgens H., Eulenberg K., Wehr R., Dohrmann C., Joost H.-G., Schürmann A. Ablation of the cholesterol transporter adenosine triphosphate-binding cassette transporter G1 reduces adipose cell size and protects against diet-induced obesity. Endocrinology 2007, 148:1561-1573.
25. Buss D.S., Callaghan A. Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pestic. Biochem. Physiol. 2008, 90:141-153.
26. Buss D.S., McCaffery A.R., Callaghan A. Evidence for P-glycoprotein modification of insecticide toxicity in mosquitoes of the Culex pipiens complex. Med. Vet. Entomol. 2002, 16:218-222.
27. Chahine S., O'Donnell M.J. Physiological and molecular characterization of methotrexate transport by Malpighian tubules of adult Drosophila melanogaster. J.Insect Physiol. 2009, 55:927-935.
28. Chahine S., O'Donnell M.J. Interactions between detoxification mechanisms and excretion in Malpighian tubules of Drosophila melanogaster. J.Exp. Biol. 2011, 214:462-468.
29. Chahine S., Seabrooke S., O'Donnell M.J. Effects of genetic knock-down of organic anion transporter genes on secretion of fluorescent organic ions by Malpighian tubules of Drosophila melanogaster. Arch. Insect Biochem. Physiol. 2012, 81:228-240.
30. Chavan H., Khan M.M.T., Tegos G., Krishnamurthy P. Efficient purification and reconstitution of ABCB6 for functional and structural studies. J.Biol. Chem. 2013, 288:22658-22669.
31. Choi C.-H. ABC transporters as multidrug resistance mechanisms and the development of chemosensitizers for their reversal. Cancer Cell Int. 2005, 5:30.
32. Cole S.P.C. Targeting multidrug resistance protein 1 (MRP1, ABCC1): past, present, and future. Annu. Rev. Pharmacol. Toxicol. 2014, 54. 10.1146/annurev-pharmtox-011613-135959.
33. Cole S., Bhardwaj G., Gerlach J., Mackie J., Grant C., Almquist K., Stewart A., Kurz E., Duncan A., Deeley R. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258:1650-1654.
34. Coleman J.J., Mylonakis E. Efflux in Fungi: La Pièce de Résistance. PLoS Pathog. 2009, 5:e1000486.
35. de Maagd R.A., Bravo A., Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. 2001, 17:193-199.
36. Dean M., Rzhetsky A., Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001, 11:1156-1166.
37. Deeley R.G., Westlake C., Cole S.P.C. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 2006, 86:849-899.
38. Dermauw W., Ilias A., Riga M., Tsagkarakou A., Grbić M., Tirry L., Van Leeuwen T., Vontas J. The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: implications for acaricide toxicology and a novel mutation associated with abamectin resistance. Insect Biochem. Mol. Biol. 2012, 42:455-465.
39. Dermauw W., Osborne E., Clark R., Grbić M., Tirry L., Van Leeuwen T. Aburst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics 2013, 14:317.
40. Dermauw W., Wybouw N., Rombauts S., Menten B., Vontas J., Grbić M., Clark R.M., Feyereisen R., Van Leeuwen T. Alink between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E113-E122.
41. Despres L., David J., Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 2007, 22:298-307.
42. Dutta S. Genetic Regulation of Autophagic Cell Death in Drosophila melanogaster 2008, University of Maryland, Department Molecular and Cell Biology, p. 130.
43. Eleftherianos I., Won S., Chtarbanova S., Squiban B., Ocorr K., Bodmer R., Beutler B., Hoffmann J.A., Imler J.-L. ATP-sensitive potassium channel (K-ATP)-dependent regulation of cardiotropic viral infections. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12024-12029.
44. Elliott A.M., Ai-Hajj M.A. ABCB8 Mediates doxorubicin resistance in melanoma cells by protecting the mitochondrial genome. Mol. Cancer Res. 2009, 7:79-87.
45. Ellis L., Carney G. Mating alters gene expression patterns in Drosophila melanogaster male heads. BMC Genomics 2010, 11:558.
46. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2:953-971.
47. Etter P., Narayanan R., Navratilova Z., Patel C., Bohmann D., Jasper H., Ramaswami M. Synaptic and genomic responses to JNK and AP-1 signaling in Drosophila neurons. BMC Neurosci. 2005, 6:39.
48. Evans J.M., Day J.P., Cabrero P., Dow J.A.T., Davies S.-A. A new role for a classical gene: white transports cyclic GMP. J. Exp. Biol. 2008, 211:890-899.
49. Ewart G.D., Howells A.J. ABC transporters involved in transport of eye pigment precursors in Drosophila melanogaster. Methods Enzymol. 1998, 213-224. Academic Press. V. Suresh, M.M.G. Ambudkar (Eds.).
50. Ewart G.D., Cannell D., Cox G.B., Howells A.J. Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster. Implications for structure-function relationships. J.Biol. Chem. 1994, 269:10370-10377.
51. Figueira-Mansur J., Ferreira-Pereira A., Mansur J.F., Franco T.A., Alvarenga E.S.L., Sorgine M.H.F., Neves B.C., Melo A.C.A., Leal W.S., Masuda H., Moreira M.F. Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Mol. Biol. 2013, 10.1111/imb.12052.
52. Gaertner L.S., Murray C.L., Morris C.E. 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. 1998, 201:2637-2645.
53. Gahan L.J., Pauchet Y., Vogel H., Heckel D.G. An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet. 2010, 6:e1001248.
54. Gangishetti U., Breitenbach S., Zander M., Saheb S.K., Mueller U., Schwarz H., Moussian B. Effects of benzoylphenylurea on chitin synthesis and orientation in the cuticle of the Drosophila larva. Eur. J. Cell Biol. 2009, 88:167-180.
55. Gardiner D.M., Stephens A.E., Munn A.L., Manners J.M. An ABC pleiotropic drug resistance transporter of Fusarium graminearum with a role in crown and root diseases of wheat. FEMS Microbiol. Lett. 2013, 348:36-45.
56. George A.M., Jones P.M. Perspectives on the structure-function of ABC transporters: the Switch and Constant Contact Models. Prog. Biophys. Mol. Biol. 2012, 109:95-107.
57. Glavinas H., Méhn D., Jani M., Oosterhuis B., Herédi-Szabó K., Krajcsi P. Utilization of membrane vesicle preparations to study drug-ABC transporter interactions. Expert Opin. Drug Metab. Toxicol. 2008, 4:721-732.
58. Govind G., Mittapalli O., Griebel T., Allmann S., Bocker S., Baldwin I.T. Unbiased transcriptional comparisons of generalist and specialist herbivores feeding on progressively defenseless Nicotiana attenuata plants. PLoS ONE 2010, 5:e8735.
59. Graf G.A., Yu L.Q., Li W.P., Gerard R., Tuma P.L., Cohen J.C., Hobbs H.H. ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion. J.Biol. Chem. 2003, 278:48275-48282.
60. Grailles M., Brey P.T., Roth C.W. The Drosophila melanogaster multidrug-resistance protein 1 (MRP1) homolog has a novel gene structure containing two variable internal exons. Gene 2003, 307:41-50.
61. 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 É., 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., Peer Y.V.d The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 2011, 479:487-492.
62. Green M.M. The 'genesis of the white-eyed mutant' in Drosophila melanogaster: a reappraisal. Genetics 1996, 142:329-331.
63. Gros P., Dhir R., Croop J., Talbot F. Asingle amino acid substitution strongly modulates the activity and substrate specificity of the mouse mdr1 and mdr3 drug efflux pumps. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:7289-7293.
64. Guo Y., Kotova E., Chen Z.-S., Lee K., Hopper-Borge E., Belinsky M.G., Kruh G.D. MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for Fluoropyrimidines 2',3'-Dideoxycytidine and 9'-(2'-Phosphonylmethoxyethyl)adenine. J.Biol. Chem. 2003, 278:29509-29514.
65. Hawthorne D.J., Dively G.P. Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees. PLoS ONE 2011, 6:e26796.
66. Heckel D.G. Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pestic. Biochem. Physiol. 2012, 104:103-110.
67. Hediger M.A., Clemencon B., Burrier R.E., Bruford E.A. The ABCs of membrane transporters in health and disease (SLC series): introduction. Mol. Asp. Med. 2013, 34:95-107.
68. Higgins C.F. ABC transporters - from microorganisms to man. Annu. Rev. Cell Biol. 1992, 8:67-113.
69. Higgins C.F., Linton K.J. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 2004, 11:918-926.
70. Hock T., Cottrill T., Keegan J., Garza D. The E23 early gene of Drosophila encodes an ecdysone-inducible ATP-binding cassette transporter capable of repressing ecdysone-mediated gene activation. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:9519-9524.
71. Hopper-Borge E., Xu X., Shen T., Shi Z., Chen Z.-S., Kruh G.D. Human Multidrug Resistance Protein 7 (ABCC10) is a resistance factor for nucleoside analogues and epothilone B. Cancer Res. 2009, 69:178-184.
72. Huang H., Haddad G.G. Drosophila dMRP4 regulates responsiveness to O-2 deprivation and development under hypoxia. Physiol. Genomics 2007, 29:260-266.
73. i5K-Consortium The i5K initiative: advancing arthropod Genomics for knowledge, human health, agriculture, and the environment. J.Hered. 2013, 104:595-600.
74. ®) resistance in sea lice, Lepeophtheirus salmonis. Aquaculture 2012, 344-349:40-47.
75. Jones C.M., Toe H.K., Sanou A., Namountougou M., Hughes A., Diabate A., Dabire R., Simard F., Ranson H. Additional selection for insecticide resistance in urban malaria vectors: DDT Resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS ONE 2012, 7.
76. Kartner N., Everndenporelle D., Bradley G., Ling V. Detection of P-glycoprotein in multidrug-resistant cell-lines by monoclonal-antibodies. Nature 1985, 316:820-823.
77. Kennedy C., Tierney K. Xenobiotic protection/resistance mechanisms inorganisms. Environ. Toxicol. 2013, 689-721. Springer, New York. E.A. Laws (Ed.).
78. Keppler D. Multidrug resistance proteins (MRPs, ABCCs): importance for pathophysiology and drug therapy. Drug Transporters 2011, 299-323. Springer, Berlin Heidelberg. M.F. Fromm, R.B. Kim (Eds.).
79. Kerboeuf D., Guégnard F. Anthelmintics are substrates and activators of nematode P-glycoprotein. Antimicrob. Agents Chemother. 2011, 55:2224-2232.
80. Kerr I.D., Haider A.J., Gelissen I.C. The ABCG family of membrane-associated transporters: you don't have to be big to be mighty. Br. J. Pharmacol. 2011, 164:1767-1779.
81. Komoto N., Quan G.-X., Sezutsu H., Tamura T. Asingle-base deletion in an ABC transporter gene causes white eyes, white eggs, and translucent larval skin in the silkworm w-3(oe) mutant. Insect Biochem. Mol. Biol. 2009, 39:152-156.
82. Kovalchuk A., Driessen A.J.M. Phylogenetic analysis of fungal ABC transporters. BMC Genomics 2010, 11:177.
83. Krumpochova P., Sapthu S., Brouwers J.F., de Haas M., de Vos R., Borst P., van de Wetering K. Transportomics: screening for substrates of ABC transporters in body fluids using vesicular transport assays. FASEB J. 2012, 26:738-747.
84. Kuwana H., Shimizu-Nishikawa K., Iwahana H., Yamamoto D. Molecular cloning and characterization of the ABC transporter expressed in Trachea (ATET) gene from Drosophila melanogaster. Biochim. Biophys. Acta 1996, 1309:47-52.
85. Labbé R., Caveney S., Donly C. Genetic analysis of the xenobiotic resistance-associated ABC gene subfamilies of the Lepidoptera. Insect Mol. Biol. 2011, 20:243-256.
86. Lanning C.L., Fine R.L., Corcoran J.J., Ayad H.M., Rose R.L., Abou-Donia M.B. Tobacco budworm P-glycoprotein: biochemical characterization and its involvement in pesticide resistance. Biochim. Biophys. Acta 1996, 1291:155-162.
87. Lanning C.L., Fine R.L., Sachs C.W., Rao U.S., Corcoran J.J., Abou-Donia M.B. Chlorpyrifos oxon interacts with the mammalian multidrug resistance protein, P-glycoprotein. J.Toxicol. Environ. Health 1996, 47:395-407.
88. Lebedeva I.V., Pande P., Patton W.F. Sensitive and specific fluorescent probes for functional analysis of the three major types of mammalian ABC transporters. PLoS ONE 2011, 6:e22429.
89. Lei Y., Zhu X., Xie W., Wu Q., Wang S., Guo Z., Xu B., Li X., Zhou X., Zhang Y. Midgut transcriptome response to a Cry toxin in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Gene 2014, 533:180-187.
90. Leslie E.M. Arsenic-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). J.Inorg. Biochem. 2012, 108:141-149.
91. Leslie E.M., Deeley R.G., Cole S.P.C. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 2005, 204:216-237.
92. Lespine A., Ménez C., Bourguinat C., Prichard R.K. P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. Int. J. Parasitol. Drugs Drug Resist. 2012, 2:58-75.
93. Lin J.H., Yamazaki M. Role of P-glycoprotein in pharmacokinetics: clinical implications. Clin. Pharmacokinet. 2003, 42:59-98.
94. Linton K.J., Higgins C.F. Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch. 2007, 453:555-567.
95. Litman T., Zeuthen T., Skovsgaard T., Stein W.D. Structure-activity relationships of P-glycoprotein interacting drugs: kinetic characterization of their effects on ATPase activity. Biochim. Biophys. Acta 1997, 1361:159-168.
96. Liu Y., Lehmann M. Agenomic response to the yeast transcription factor GAL4 in Drosophila. Fly (Austin) 2008, 2:92-98.
97. Liu R., Siemiarczuk A., Sharom F.J. Intrinsic fluorescence of the P-glycoprotein multidrug transporter: sensitivity of tryptophan residues to binding of drugs and nucleotides. Biochemistry 2000, 39:14927-14938.
98. Liu S., Zhou S., Tian L., Guo E., Luan Y., Zhang J., Li S. Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori. BMC Genomics 2011, 12.
99. Liu W., Feng Q., Li Y., Ye L., Hu M., Liu Z. Coupling of UDP-glucuronosyltransferases and multidrug resistance-associated proteins is responsible for the intestinal disposition and poor bioavailability of emodin. Toxicol. Appl. Pharmacol. 2012, 265:316-324.
100. Liu S., Li Q., Liu Z. Genome-wide identification, characterization and phylogenetic analysis of 50 catfish ATP-binding cassette (ABC) transporter genes. PLoS ONE 2013, 8:e63895.
101. Loe D.W., Deeley R.G., Cole S.P.C. Characterization of vincristine transport by the Mr 190,000 Multidrug Resistance Protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res. 1998, 58:5130-5136.
102. Loe D.W., Deeley R.G., Cole S.P.C. Verapamil stimulates glutathione transport by the 190-kDa Multidrug Resistance Protein 1 (MRP1). J.Pharmacol. Exp. Ther. 2000, 293:530-538.
103. Lorenzen M.D., Brown S.J., Denell R.E., Beeman R.W. Cloning and characterization of the Tribolium castaneum eye-color genes encoding tryptophan oxygenase and kynurenine 3-monooxygenase. Genetics 2002, 160:225-234.
104. Luo L., Sun Y.-J., Wu Y.-J. Abamectin resistance in Drosophila is related to increased expression of P-glycoprotein via the dEGFR and dAkt pathways. Insect Biochem. Mol. Biol. 2013, 43:627-634.
105. Luo L., Sun Y.-J., Yang L., Huang S., Wu Y.-J. Avermectin induces P-glycoprotein expression in S2 cells via the calcium/calmodulin/NF-κB pathway. Chem. Biol. Interact. 2013, 203:430-439.
106. Mackenzie S.M., Brooker M.R., Gill T.R., Cox G.B., Howells A.J., Ewart G.D. Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. Biochim. Biophys. Acta 1999, 1419:173-185.
107. Mamidala P., Wijeratne A., Wijeratne S., Kornacker K., Sudhamalla B., Rivera-Vega L., Hoelmer A., Meulia T., Jones S., Mittapalli O. RNA-Seq and molecular docking reveal multi-level pesticide resistance in the bed bug. BMC Genomics 2012, 13:6.
108. Martin S., Oduola A., Milhous W. Reversal of chloroquine resistance in Plasmodium falciparum by verapamil. Science 1987, 235:899-901.
109. Martin A., Saathoff M., Kuhn F., Max H., Terstegen L., Natsch A. Afunctional ABCC11 Allele is essential in the biochemical formation of human Axillary Odor. J.Invest. Dermatol. 2009, 130:529-540.
110. Matsumura F. Studies on the action mechanism of benzoylurea insecticides to inhibit the process of chitin synthesis in insects: a review on the status of research activities in the past, the present and the future prospects. Pestic. Biochem. Physiol. 2010, 97:133-139.
111. Mayer F., Mayer N., Chinn L., Pinsonneault R.L., Kroetz D., Bainton R.J. Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J.Neurosci. 2009, 29:3538-3550.
112. Merzendorfer H., Kim H.S., Chaudhari S.S., Kumari M., Specht C.A., Butcher S., Brown S.J., Robert Manak J., Beeman R.W., Kramer K.J., Muthukrishnan S. Genomic and proteomic studies on the effects of the insect growth regulator diflubenzuron in the model beetle species Tribolium castaneum. Insect Biochem. Mol. Biol. 2012, 42:264-276.
113. Meyer F., Flötenmeyer M., Moussian B. The sulfonylurea receptor SUR is dispensable for chitin synthesis in Drosophila melanogaster embryos. Pest Manag. Sci. 2012, 69:1136-1140.
114. Misra J.R., Horner M.A., Lam G., Thummel C.S. Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev. 2011, 25:1796-1806.
115. Morgan T.H. Sex limited inheritance in Drosophila. Science 1910, 32:120-122.
116. Morita M., Imanaka T. Peroxisomal ABC transporters: structure, function and role in disease. Biochim. Biophys. Acta 2012, 1822:1387-1396.
117. Mounsey, K.E., Holt, D.C., McCarthy, J., Currie, B., Walton, S.F., 2007. Expression of candidate ivermectin resistance genes in the scabies mite Sarcoptes scabiei. In: 3rd International qPCR Symposium & Industrial Exhibition & Application Workshop, Munich.
118. Mounsey K.E., Holt D.C., McCarthy J., Walton S.F. Identification of ABC transporters in Sarcoptes scabiei. Parasitology 2006, 132:883-892.
119. Mount S.M. Sequence similarity. Nature 1987, 325:487.
120. Mummery-Widmer J.L., Yamazaki M., Stoeger T., Novatchkova M., Bhalerao S., Chen D., Dietzl G., Dickson B.J., Knoblich J.A. Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 2009, 458:U987-U992.
121. Murray C.L., Quaglia M., Arnason J.T., Morris C.E. Aputative nicotine pump at the metabolic blood-brain-barrier of the tobacco hornworm. J.Neurobiol. 1994, 25:23-34.
122. Nasonkin I., Alikasifoglu A., Ambrose C., Cahill P., Cheng M., Sarniak A., Egan M., Thomas P.M. Anovel sulfonylurea receptor family member expressed in the embryonic Drosophila dorsal vessel and tracheal system. J.Biol. Chem. 1999, 274:29420-29425.
123. Ohmann E. Untersuchung zur Funktion und Bedeutung der ABC-Transporter in Drosophila melanogaster 2012, PhD, Universität Regensburg, p. 164.
124. Paytubi S., Wang X., Lam Y.W., Izquierdo L., Hunter M.J., Jan E., Hundal H.S., Proud C.G. ABC50 promotes translation initiation in mammalian cells. J.Biol. Chem. 2009, 284:24061-24073.
125. Pedra J.H.F., McIntyre L.M., Scharf M.E., Pittendrigh B.R. Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:7034-7039.
126. Petschenka G., Pick C., Wagschal V., Dobler S. Functional evidence for physiological mechanisms to circumvent neurotoxicity of cardenolides in an adapted and a non-adapted hawk-moth species. Proc. R. Soc. B Biol. Sci. 2013, 280.
127. Podsiadlowski L., Matha V., Vilcinskas A. Detection of a P-glycoprotein related pump in Chironomus larvae and its inhibition by verapamil and cyclosporin A. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1998, 121:443-450.
128. Pohl P.C., Klafke G.M., Carvalho D.D., Martins J.R., Daffre S., Vaz I.d.S., Masuda A. ABC transporter efflux pumps: a defense mechanism against ivermectin in Rhipicephalus (Boophilus) microplus. Int. J. Parasitol. 2011, 41:1323-1333.
129. Pohl P.C., Klafke G., Júnior J., Martins J., Silva Vaz I., Masuda A. ABC transporters as a multidrug detoxification mechanism in Rhipicephalus (Boophilus) microplus. Parasitol. Res. 2012, 111:2345-2351.
130. Popovic M., Zaja R., Loncar J., Smital T. Anovel ABC transporter: the first insight into zebrafish (Danio rerio) ABCH1. Mar. Environ. Res. 2010, 69:S11-S13.
131. Porretta D., Gargani M., Bellini R., Medici A., Punelli F., Urbanelli S. Defence mechanisms against insecticides temephos and diflubenzuron in the mosquito Aedes caspius: the P-glycoprotein efflux pumps. Med. Vet. Entomol. 2008, 22:48-54.
132. Post L.C., Vincent W.R. Anew insecticide inhibits chitin synthesis. Naturwissenschaften 1973, 60:431-432.
133. Pouliot J.-F., L'Heureux F., Liu Z., Prichard R.K., Georges E. Reversal of P-glycoprotein-associated multidrug resistance by ivermectin. Biochem. Pharmacol. 1997, 53:17-25.
134. Proctor W., Ming X., Thakker D. Invitro techniques to study drug-drug interactions involving transport: Caco-2 model for study of P-glycoprotein and other transporters. Enzyme- and Transporter-based Drug-Drug Interactions 2010, 257-282. Springer, New York. K.S. Pang, A.D. Rodrigues, R.M. Peter (Eds.).
135. Pu X., Yang Y., Wu S., Wu Y. Characterisation of abamectin resistance in a field-evolved multiresistant population of Plutella xylostella. Pest Manag. Sci. 2010, 66:371-378.
136. Qin W., Neal S.J., Robertson R.M., Westwood J.T., Walker V.K. Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol. Biol. 2005, 14:607-613.
137. Rees D.C., Johnson E., Lewinson O. ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 2009, 10:218-227.
138. Reid G., Wielinga P., Zelcer N., De Haas M., Van Deemter L., Wijnholds J., Balzarini J., Borst P. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol. Pharmacol. 2003, 63:1094-1103.
139. Ricardo S., Lehmann R. An ABC transporter controls export of a Drosophila germ cell attractant. Science 2009, 323:943-946.
140. Riordan J.R., Deuchars K., Kartner N., Alon N., Trent J., Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian-cell lines. Nature 1985, 316:817-819.
141. Robert J.A., Pitt C., Bonnett T.R., Yuen M.M.S., Keeling C.I., Bohlmann J., Huber D.P.W. Disentangling detoxification: gene expression analysis of feeding mountain pine beetle illuminates molecular-level host chemical defense detoxification mechanisms. PLoS ONE 2013, 8:e77777.
142. Roth C.W., Holm I., Graille M., Dehoux P., Rzhetsky A., Wincker P., Weissenbach J., Brey P.T. Identification of the Anopheles gambiae ATP-binding cassette transporter superfamily genes. Mol. Cell 2003, 15:150-158.
143. Sau A., Pellizzari Tregno F., Valentino F., Federici G., Caccuri A.M. Glutathione transferases and development of new principles to overcome drug resistance. Arch. Biochem. Biophys. 2010, 500:116-122.
144. Schinkel A.H., Jonker J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug Delivery. Rev. 2003, 55:3-29.
145. Schinkel A.H., Smit J.J.M., van Tellingen O., Beijnen J.H., Wagenaar E., van Deemter L., Mol C.A.A.M., van der Valk M.A., Robanus-Maandag E.C., te Riele H.P.J., Berns A.J.M., Borst P. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994, 77:491-502.
146. Seelig A., Landwojtowicz E. Structure-activity relationship of P-glycoprotein substrates and modifiers. Eur. J. Pharm. Sci. 2000, 12:31-40.
147. Shah S., Yarrow C., Dunning R., Cheek B., Vass S., Windass J., Hadfield S. Insecticide detoxification indicator strains as tools for enhancing chemical discovery screens. Pest Manag. Sci. 2012, 68:38-48.
148. Sharom F.J., Liu R., Qu Q., Romsicki Y. Exploring the structure and function of the P-glycoprotein multidrug transporter using fluorescence spectroscopic tools. Semin. Cell Dev. Biol. 2001, 12:257-265.
149. Shi H., Pei L., Gu S., Zhu S., Wang Y., Zhang Y., Li B. Glutathione S-transferase (GST) genes in the red flour beetle, Tribolium castaneum, and comparative analysis with five additional insects. Genomics 2012, 100:327-335.
150. Silva A.X., Jander G., Samaniego H., Ramsey J.S., Figueroa C.C. Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) I: a transcriptomic survey. PLoS ONE 2012, 7:e36366.
151. Simmons J., D'Souza O., Rheault M., Donly C. Multidrug resistance protein gene expression in Trichoplusia ni caterpillars. Insect Mol. Biol. 2013, 22:62-71.
152. Smith A.J., van Helvoort A., van Meer G., Szabó K., Welker E., Szakács G., Váradi A., Sarkadi B., Borst P. MDR3 P-glycoprotein, a phosphatidylcholine translocase, transports several cytotoxic drugs and directly Interacts with drugs as judged by Interference with nucleotide trapping. J.Biol. Chem. 2000, 275:23530-23539.
153. Sooksa-Nguan T., Yakubov B., Kozlovskyy V.I., Barkume C.M., Howe K.J., Thannhauser T.W., Rutzke M.A., Hart J.J., Kochian L.V., Rea P.A., Vatamaniuk O.K. Drosophila ABC transporter, DmHMT-1, confers tolerance to cadmium: DmHMT-1 and its yeast homolog, SpHMT-1, are not essential for vacuolar phytochelatin sequestration. J.Biol. Chem. 2009, 284:354-362.
154. Sorensen J., Dearing M.D. Efflux transporters as a novel herbivore counter mechanism to plant chemical defenses. J.Chem. Ecol. 2006, 32:1181-1196.
155. Sreeramulu K., Liu R., Sharom F.J. Interaction of insecticides with mammalian P-glycoprotein and their effect on its transport function. Biochim. Biophys. Acta 2007, 1768:1750-1757.
156. Srinivas R., Udikeri S.S., Jayalakshmi S.K., Sreeramulu K. Identification of factors responsible for insecticide resistance in Helicoverpa armigera. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2004, 137:261-269.
157. Srinivas R., Shamsundar G.S., Jayalakshmi S.K., Sreermalu K. Effect of insecticides and inhibitors on P-glycoprotein ATPase (M-type) activity of resistant pest Helicoverpa armigera. Curr. Sci. 2005, 88:1449-1452.
158. Steck T.L., Kant J.A. Cation-impermeable inside-out and right-side-out vesicles from human erythrocyte membranes. Nature 1972, 240:26-28.
159. Strycharz J.P. Polygenic Resistance in the Highly DDT-resistant 91-R Strain of Drosophila melanogaster Involves Decreased Penetration, Increased Metabolism and Direct Excretion of DDT 2010, University of Massachusetts. Department of Veterinary and Animal Sciences, p. 83.
160. Strycharz J.P., Lee S.H., Sun W., Pittendrigh B.R., Clark J.M. RNAi Knockdown of ABC Transporters Causes Decreased Tolerance in the Highly DDT-resistant 91-R Strain of Drosophila melanogaster. Picogram, Abstract Book 2010, vol. 78. p. 116.
161. Strycharz J.P., Lao A., Li H., Qiu X., Lee S.H., Sun W., Yoon K.S., Doherty J.J., Pittendrigh B.R., Clark J.M. Resistance in the highly DDT-resistant 91-R strain of Drosophila melanogaster involves decreased penetration, increased metabolism, and direct excretion. Pestic. Biochem. Physiol. 2013, 107:207-217.
162. Sturm A., Cunningham P., Dean M. The ABC transporter gene family of Daphnia pulex. BMC Genomics 2009, 10.
163. Szeri F., Ilias A., Pomozi V., Robinow S., Bakos E., Varadi A. The high turnover Drosophila multidrug resistance-associated protein shares the biochemical features of its human orthologues. Biochim. Biophys. Acta 2009, 1788:402-409.
164. Tabashnik B.E., Brevault T., Carriere Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat. Biotech. 2013, 31:510-521.
165. Tanaka S., Miyamoto K., Noda H., Jurat-Fuentes J.L., Yoshizawa Y., Endo H., Sato R. The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. FEBS J. 2013, 280:1782-1794.
166. Tapadia M.G., Lakhotia S.C. Expression of mdr49 and mdr65 multidrug resistance genes in larval tissues of Drosophila melanogaster under normal and stress conditions. Cell Stress Chaperones 2005, 10:7-11.
167. Tarnay J.N., Szeri F., Ilias A., Annilo T., Sung C., Le Saux O., Varadi A., Dean M., Boyd C.D., Robinow S. The dMRP/CG6214 gene of Drosophila is evolutionarily and functionally related to the human multidrug resistance-associated protein family. Insect Mol. Biol. 2004, 13:539-548.
168. Tarr P.T., Tarling E.J., Bojanic D.D., Edwards P.A., Baldan A. Emerging new paradigms for ABCG transporters. Biochim. Biophys. Acta 2009, 1791:584-593.
169. Tatematsu K.-i., Yamamoto K., Uchino K., Narukawa J., Iizuka T., Banno Y., Katsuma S., Shimada T., Tamura T., Sezutsu H., Daimon T. Positional cloning of silkworm white egg 2 (w-2) locus shows functional conservation and diversification of ABC transporters for pigmentation in insects. Genes Cells 2011, 16:331-342.
170. Telonis-Scott M., Hallas R., McKechnie S.W., Wee C.W., Hoffmann A.A. Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. J.Insect Physiol. 2009, 55:549-555.
171. Tribble N.D., Burka J.F., Kibenge F.S.B. Evidence for changes in the transcription levels of two putative P-glycoprotein genes in sea lice (Lepeophtheirus salmonis) in response to emamectin benzoate exposure. Mol. Biochem. Parasitol. 2007, 153:59-65.
172. Trowsdale J., Hanson I., Mockridge I., Beck S., Townsendt A., Kelly A. Sequences encoded in the class II region of the MHC related to the 'ABC' superfamily of transporters. Nature 1990, 348:741-744.
173. Urbatsch I.L., Sankaran B., Weber J., Senior A.E. P-glycoprotein Is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J.Biol. Chem. 1995, 270:19383-19390.
174. Vaché C., Camares O., De Graeve F., Dastugue B., Meiniel A., Vaury C., Pellier S., Leoz-Garziandia E., Bamdad M. Drosophila melanogaster P-glycoprotein: a membrane detoxification system toward polycyclic aromatic hydrocarbon pollutants. Environ. Toxicol. Chem. 2006, 25:572-580.
175. Vaché C., Camares O., Marie C., Cardoso F., Dastugue B., Creveaux I., Vaury C., Bamdad M. Apotential genomic biomarker for the detection of polycyclic aromatic hydrocarbon pollutants: multidrug resistance gene 49 in Drosophila melanogaster. Environ. Toxicol. Chem. 2007, 26:1418-1424.
176. Van Leeuwen T., Demaeght P., Osborne E.J., Dermauw W., Gohlke S., Nauen R., Grbić M., Tirry L., Merzendorfer H., Clark R.M. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4407-4412.
177. Verrier P.J., Bird D., Buria B., Dassa E., Forestier C., Geisler M., Klein M., Kolukisaoglu U., Lee Y., Martinoia E., Murphy A., Rea P.A., Samuels L., Schulz B., Spalding E.P., Yazaki K., Theodoulou F.L. Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci. 2008, 13:151-159.
178. Waterhouse R.M., Zdobnov E.M., Tegenfeldt F., Li J., Kriventseva E.V. OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Res. 2011, 39:D283-D288.
179. Wenzel J.J., Piehler A., Kaminski W.E. ABC A-subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport. Front. Biosci. 2007, 12:3177-3193.
180. Wolstenholme A.J., Kaplan R.M. Resistance to macrocyclic lactones. Curr. Pharm. Biotechnol. 2012, 13:873-887.
181. Wu C.T., Budding M., Griffin M.S., Croop J.M. Isolation and characterization of Drosophila multidrug resistance gene homologs. Mol. Cell. Biol. 1991, 11:3940-3948.
182. Xie X., Cheng T., Wang G., Duan J., Niu W., Xia Q. Genome-wide analysis of the ATP-binding cassette (ABC) transporter gene family in the silkworm, Bombyx mori. Mol. Biol. Rep. 2012, 39:7281-7291.
183. Yadav S., Tapadia M.G. Neurodegeneration caused by polyglutamine expansion is regulated by P-glycoprotein in Drosophila melanogaster. Genetics 2013, 195:857-870.
184. Yang N., Xie W., Jones C.M., Bass C., Jiao X., Yang X., Liu B., Li R., Zhang Y. Transcriptome profiling of the whitefly Bemisia tabaci reveals stage-specific gene expression signatures for thiamethoxam resistance. Insect Mol. Biol. 2013, 22:485-496.
185. Yang N., Xie W., Yang X., Wang S., Wu Q., Li R., Pan H., Liu B., Shi X., Fang Y., Xu B., Zhou X., Zhang Y. Transcriptomic and proteomic responses of sweetpotato whitefly, Bemisia tabaci, to thiamethoxam. PLoS ONE 2013, 8:e61820.
186. Yepiskoposyan H., Egli D., Fergestad T., Selvaraj A., Treiber C., Multhaup G., Georgiev O., Schaffner W. Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res. 2006, 34:4866-4877.
187. Yoon K.S., Strycharz J.P., Baek J.H., Sun W., Kim J.H., Kang J.S., Pittendrigh B.R., Lee S.H., Clark J.M. Brief exposures of human body lice to sublethal amounts of ivermectin over-transcribes detoxification genes involved in tolerance. Insect Mol. Biol. 2011, 20:687-699.
188. Yoshiura K., Kinoshita A., Ishida T., Ninokata A., Ishikawa T., Kaname T., Bannai M., Tokunaga K., Sonoda S., Komaki R., Ihara M., Saenko V.A., Alipov G.K., Sekine I., Komatsu K., Takahashi H., Nakashima M., Sosonkina N., Mapendano C.K., Ghadami M., Nomura M., Liang D.S., Miwa N., Kim D.K., Garidkhuu A., Natsume N., Ohta T., Tomita H., Kaneko A., Kikuchi M., Russomando G., Hirayama K., Ishibashi M., Takahashi A., Saitou N., Murray J.C., Saito S., Nakamura Y., Niikawa N. ASNP in the ABCC11 gene is the determinant of human earwax type. Nat. Genet. 2006, 38:324-330.
189. You M., Yue Z., He W., Yang X., Yang G., Xie M., Zhan D., Baxter S.W., Vasseur L., Gurr G.M., Douglas C.J., Bai J., Wang P., Cui K., Huang S., Li X., Zhou Q., Wu Z., Chen Q., Liu C., Wang B., Li X., Xu X., Lu C., Hu M., Davey J.W., Smith S.M., Chen M., Xia X., Tang W., Ke F., Zheng D., Hu Y., Song F., You Y., Ma X., Peng L., Zheng Y., Liang Y., Chen Y., Yu L., Zhang Y., Liu Y., Li G., Fang L., Li J., Zhou X., Luo Y., Gou C., Wang J., Wang J., Yang H., Wang J. Aheterozygous moth genome provides insights into herbivory and detoxification. Nat. Genet. 2013, 45:220-225.
190. Zhang S.D., Odenwald W.F. Misexpression of the white (omega) gene triggers male-made courtship in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:5525-5529.
191. Zhang Y., Bachmeier C., Miller D.W. Invitro and invivo models for assessing drug efflux transporter activity. Adv. Drug Delivery. Rev. 2003, 55:31-51.
192. Zhang S., Feany M.B., Saraswati S., Littleton J.T., Perrimon N. Inactivation of Drosophila Huntingtin affects long-term adult functioning and the pathogenesis of a Huntington's disease model. Dis. Model. Mech. 2009, 2:247-266.
193. Zhu F., Gujar H., Gordon J.R., Haynes K.F., Potter M.F., Palli S.R. Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci. Rep. 2013, 3.
194. Zutz A., Gompf S., Schaegger H., Tampe R. Mitochondrial ABC proteins in health and disease. Biochim. Biophys. Acta 2009, 1787:681-690.