A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Dermauw, Wannes ^a   Osborne, Edward John ^b   Clark, Richard M ^b   Grbić, Miodrag ^c,d   Tirry, Luc ^a   Van Leeuwen, Thomas ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d UNIVERSITY OF LA RIOJA   (Spain)

Author keywords

Acari; Duplication; Major facilitator superfamily; Microarray; Phase III detoxification; RNA seq

Indexed keywords

ABC TRANSPORTER; ECDYSONE; ECDYSONE REGULATED TRANSPORTER E23; SULFONYLUREA RECEPTOR; UNCLASSIFIED DRUG;

ABC GENE; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENOME; HUMAN; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHYLOGENY; TETRANYCHUS URTICAE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; EVOLUTION, MOLECULAR; GENOMICS; HUMANS; PHYLOGENY; TETRANYCHIDAE; TRANSCRIPTOME;

ACARI; ARTHROPODA; CRUSTACEA; DROSOPHILA MELANOGASTER; HEXAPODA; INVERTEBRATA; METAZOA; TETRANYCHIDAE; TETRANYCHUS URTICAE; VERTEBRATA;

EID: 84877300013     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-317     Document Type: Article

References (133)

1. Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 2001, 11:1156-1166. 10.1101/gr.GR-1649R, 11435397.
2. Higgins CF. ABC transporters - from microorganisms to man. Annu Rev Cell Biol 1992, 8:67-113. 10.1146/annurev.cb.08.110192.000435, 1282354.
3. Hollenstein K, Dawson RJP, Locher KP. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 2007, 17:412-418. 10.1016/j.sbi.2007.07.003, 17723295.
4. Rees DC, Johnson E, Lewinson O. ABC transporters: the power to change. Nat Rev Mol Cell Biol 2009, 10:218-227. 10.1038/nrm2646, 2830722, 19234479.
5. Pao SS, Paulsen IT, Saier MH. Major facilitator superfamily. Microbiol Mol Biol Rev 1998, 62:1-34. 98904, 9529885.
6. Dean M, Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annual Review of Genomics and Human Genetics Vol 6 2005, 123-142. California: Palo Alto: Annual Review of Genomics and Human Genetics, Page DS, Chakravarti A.
7. Annilo T, Chen ZQ, Shulenin S, Costantino J, Thomas L, Lou H, Stefanov S, Dean M. Evolution of the vertebrate ABC gene family: Analysis of gene birth and death. Genomics 2006, 88:1-11. 10.1016/j.ygeno.2006.03.001, 16631343.
8. 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, 14:6. 10.1186/1471-2164-14-6, 3560195, 23324493.
9. 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, 12:491. 10.1186/1471-2164-12-491, 3224256, 21981826.
10. Popovic M, Zaja R, Loncar J, Smital T. A novel ABC transporter: the first insight into zebrafish (Danio rerio) ABCH1. Mar Environ Res 2010, 69:S11-S13.
11. Sturm A, Cunningham P, Dean M. The ABC transporter gene family of Daphnia pulex. BMC Genomics 2009, 10:170. 10.1186/1471-2164-10-170, 2680897, 19383151.
12. 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. 10.1007/s11033-012-1558-3, 22311044.
13. You M, Yue Z, He W, Yang X, Yang G, Xie M, Zhan D, Baxter SW, Vasseur L, Gurr GM. A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 2013, 45:220-225. 10.1038/ng.2524, 23313953.
14. 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. 10.1111/j.1365-2583.2010.01064.x, 21199020.
15. Kovalchuk A, Driessen AJM. Phylogenetic analysis of fungal ABC transporters. BMC Genomics 2010, 11:177. 10.1186/1471-2164-11-177, 2848647, 20233411.
16. Roth CW, Holm I, Graille M, Dehoux P, Rzhetsky A, Wincker P, Weissenbach J, Brey PT. Identification of the Anopheles gambiae ATP-binding cassette transporter superfamily genes. Mol Cells 2003, 15:150-158.
17. Borst P, Elferink RO. Mammalian ABC transporters in health and disease. Annu Rev Biochem 2002, 71:537-592. 10.1146/annurev.biochem.71.102301.093055, 12045106.
18. Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldan A. Emerging new paradigms for ABCG transporters. Biochim Biophys Acta Mol Cell Biol Lipids 2009, 1791:584-593.
19. Fukuda Y, Schuetz JD. ABC transporters and their role in nucleoside and nucleotide drug resistance. Biochem Pharmacol 2012, 83:1073-1083. 10.1016/j.bcp.2011.12.042, 3319017, 22285911.
20. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Delivery Rev 2003, 55:3-29.
21. Ricardo S, Lehmann R. An ABC transporter controls export of a Drosophila germ cell attractant. Science 2009, 323:943-946. 10.1126/science.1166239, 2729540, 19213920.
22. Mackenzie SM, Brooker MR, Gill TR, Cox GB, Howells AJ, Ewart GD. Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. Biochim Biophys Acta Biomembranes 1999, 1419:173-185.
23. Komoto N, Quan G-X, Sezutsu H, Tamura T. A single-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. 10.1016/j.ibmb.2008.10.003, 18996197.
24. Gaertner LS, Murray CL, Morris CE. 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.
25. Murray CL, Quaglia M, Arnason JT, Morris CE. A putative nicotine pump at the metabolic blood-brain-barrier of the tobacco hornworm. J Neurobiol 1994, 25:23-34. 10.1002/neu.480250103, 7906712.
26. Buss DS, 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.
27. Heckel DG. 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.
28. Lanning CL, Fine RL, Corcoran JJ, Ayad HM, Rose RL, AbouDonia MB. Tobacco budworm P-glycoprotein: biochemical characterization and its involvement in pesticide resistance. Biochim Biophys Acta Gen Subj 1996, 1291:155-162.
29. Baxter SW, Badenes-Perez FR, Morrison A, Vogel H, Crickmore N, Kain W, Wang P, Heckel DG, Jiggins CD. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 2011, 189:675-U814. 10.1534/genetics.111.130971, 3189815, 21840855.
30. Li X, Schuler M, Berenbaum M. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 2007, 52:231-253. 10.1146/annurev.ento.51.110104.151104, 16925478.
31. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L. Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochem Mol Biol 2010, 40:563-572. 10.1016/j.ibmb.2010.05.008, 20685616.
32. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 2006, 15:615-636. 10.1111/j.1365-2583.2006.00672.x, 1761136, 17069637.
33. Oakeshott JG, Johnson RM, Berenbaum MR, Ranson H, Cristino AS, Claudianos C. Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Mol Biol 2010, 19:147-163.
34. Ramsey JS, Rider DS, Walsh TK, De Vos M, Gordon KHJ, Ponnala L, Macmil SL, Roe BA, Jander G. Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Mol Biol 2010, 19:155-164.
35. Mounsey KE, Holt DC, McCarthy J, Walton SF. Identification of ABC transporters in Sarcoptes scabiei. Parasitology 2006, 132:883-892. 10.1017/S0031182005009716, 16454864.
36. Walter DE, Proctor HC. Mites: Ecology, Evolution and Behaviour 1999, London: CABI Publishing.
37. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Ngoc PCT, Ortego F. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 2011, 479:487-492. 10.1038/nature10640, 22113690.
38. Jeppson LR, Keifer HH, Baker EW. Mites injurious to Economic Plants 1975, Berkeley, Los Angeles: University of California Press.
39. Spider Mites Web: a comprehensive database for the Tetranychidae http://www.montpellier.inra.fr/CBGP/spmweb.
40. Arthropod Pesticide Resistance Database http://www.pesticideresistance.org.
41. Yang XM, Buschman LL, Zhu KY, Margolies DC. Susceptibility and detoxifying enzyme activity in two spider mite species (Acari : Tetranychidae) after selection with three insecticides. J Econ Entomol 2002, 95:399-406. 10.1603/0022-0493-95.2.399, 12020020.
42. Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbić M, Clark RM, Feyereisen R, Van Leeuwen T. A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc Natl Acad Sci USA 2013, 110:E113-E122. 10.1073/pnas.1213214110, 3545796, 23248300.
43. Van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S, Nauen R, Grbic M, Tirry L, Merzendorfer H, Clark RM. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci USA 2012, 109:4407-4412. 10.1073/pnas.1200068109, 3311382, 22393009.
44. Van Leeuwen T, Dermauw W, Grbic M, Tirry L, Feyereisen R. Spider mite control and resistance management: does a genome help?. Pest Manag Sci 2013, 69:156-159. 10.1002/ps.3335, 22696491.
45. Sheps JA, Ralph S, Zhao ZY, Baillie DL, Ling V. The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol 2004, 5:R15. 10.1186/gb-2004-5-3-r15, 395765, 15003118.
46. Xiong J, Feng L, Yuan D, Fu C, Miao W. Genome-wide identification and evolution of ATP-binding cassette transporters in the ciliate Tetrahymena thermophila: A case of functional divergence in a multigene family. BMC Evol Biol 2010, 10:330. 10.1186/1471-2148-10-330, 2984421, 20977778.
47. Verrier PJ, Bird D, Buria B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E. Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci 2008, 13:151-159. 10.1016/j.tplants.2008.02.001, 18299247.
48. Peelman F, Labeur C, Vanloo B, Roosbeek S, Devaud C, Duverger N, Denefle P, Rosier M, Vandekerckhove J, Rosseneu M. Characterization of the ABCA transporter subfamily: Identification of prokaryotic and eukaryotic members, phylogeny and topology. J Mol Biol 2003, 325:259-274. 10.1016/S0022-2836(02)01105-1, 12488094.
49. Beers MF, Hawkins A, Shuman H, Zhao M, Newitt JL, Maguire JA, Ding W, Mulugeta S. A novel conserved targeting motif found in ABCA transporters mediates trafficking to early post-Golgi compartments. J Lipid Res 2011, 52:1471-1482. 10.1194/jlr.M013284, 3139239, 21586796.
50. Dutta S. Genetic regulation of autophagic cell death in Drosophila melanogaster 2008, College Park: University of Maryland, Department Molecular and Cell Biology, PhD thesis.
51. Wu YC, Horvitz HR. The C. elegans cell corpse engulfment gene ced-7 encodes a protein similar to ABC transporters. Cell 1998, 93:951-960. 10.1016/S0092-8674(00)81201-5, 9635425.
52. Baycin-Hizal D, Tian Y, Akan I, Jacobson E, Clark D, Chu J, Palter K, Zhang H, Betenbaugh MJ. GlycoFly: a database of Drosophila N-linked glycoproteins identified using SPEG-MS techniques. J Proteome Res 2011, 10:2777-2784. 10.1021/pr200004t, 21480662.
53. Zarubica A, Trompier D, Chimini G. ABCA1, from pathology to membrane function. Pflueg Arch Eur J Physiol 2007, 453:569-579.
54. Akiyama M, Sugiyama-Nakagiri Y, Sakai K, McMillan JR, Goto M, Arita K, Tsuji-Abe Y, Tabata N, Matsuoka K, Sasaki R. Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest 2005, 115:1777-1784. 10.1172/JCI24834, 1159149, 16007253.
55. Albrecht C, Viturro E. The ABCA subfamily - gene and protein structures, functions and associated hereditary diseases. Pflueg Arch Eur J Physiol 2007, 453:581-589.
56. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, Bainton RJ. Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 2009, 29:3538-3550. 10.1523/JNEUROSCI.5564-08.2009, 3040577, 19295159.
57. Strycharz JP. Polygenic resistance in the highly DDT-resistant 91-R strain of Drosophila melanogaster involves decreased penetration, increased metabolism and direct excretion of DDT 2010, Department of Veterinary and Animal Sciences: M.S. University of Massachussets.
58. Lespine A, Ménez C, Bourguinat C, Prichard RK. 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.
59. Pohl PC, Klafke GM, Carvalho DD, Martins JR, Daffre S, IdS V, Masuda A. ABC transporter efflux pumps: A defense mechanism against ivermectin in Rhipicephalus (Boophilus) microplus. Int J Parasitol 2011, 41:1323-1333. 10.1016/j.ijpara.2011.08.004, 22036897.
60. Yoon KS, Strycharz JP, Baek JH, Sun W, Kim JH, Kang JS, Pittendrigh BR, Lee SH, Clark JM. 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. 10.1111/j.1365-2583.2011.01097.x, 3208734, 21895817.
61. Zutz A, Gompf S, Schaegger H, Tampe R. Mitochondrial ABC proteins in health and disease. Biochim Biophys Acta Bioenerg 2009, 1787:681-690.
62. Gonzalez-Cabo P, Bolinches-Amoros A, Cabello J, Ros S, Moreno S, Baylis HA, Palau F, Vazquez-Manrique RP. Disruption of the ATP-binding cassette B7 (ABTM-1/ABCB7) induces oxidative stress and premature cell death in Caenorhabditis elegans. J Biol Chem 2011, 286:21304-21314. 10.1074/jbc.M110.211201, 3122190, 21464130.
63. Bariami V, Jones CM, 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. 10.1371/journal.pntd.0001692, 3373657, 22720108.
64. Elliott AM, Ai-Hajj MA. ABCB8 Mediates doxorubicin resistance in melanoma cells by protecting the mitochondrial genome. Mol Canc Res 2009, 7:79-87.
65. Sachrajda I, Ratajewski M. Mithramycin A suppresses expression of the human melanoma-associated gene ABCB8. Mol Genet Genomics 2011, 285:57-65. 10.1007/s00438-010-0586-8, 21046154.
66. Ichikawa Y, Bayeva M, Ghanefar M, Potini V, Sun L, Mutharasan RK, Wu R, Khechaduri A, Naik TJ, Ardehali H. Disruption of ATP-binding cassette B8 in mice leads to cardiomyopathy through a decrease in mitochondrial iron export. Proc Natl Acad Sci USA 2012, 109:4152-4157. 3306722, 22375032.
67. Kiss K, Brozik A, Kucsma N, Toth A, Gera M, Berry L, Vallentin A, Vial H, Vidal M, Szakacs G. Shifting the paradigm: the putative mitochondrial protein ABCB6 resides in the lysosomes of cells and in the plasma membrane of erythrocytes. PLoS One 2012, 7:e37378. 10.1371/journal.pone.0037378, 3360040, 22655043.
68. Akrouh A, Halcomb SE, Nichols CG, Sala-Rabanal M. Molecular biology of K-ATP channels and implications for health and disease. IUBMB Life 2009, 61:971-978. 10.1002/iub.246, 3241984, 19787700.
69. Jordan IK, Kota KC, Cui G, Thompson CH, McCarty NA. Evolutionary and functional divergence between the cystic fibrosis transmembrane conductance regulator and related ATP-binding cassette transporters. Proc Natl Acad Sci USA 2008, 105:18865-18870. 10.1073/pnas.0806306105, 2585040, 19020075.
70. Kruh GD, Belinsky MG. The MRP family of drug efflux pumps. Oncogene 2003, 22:7537-7552. 10.1038/sj.onc.1206953, 14576857.
71. Deeley RG, Westlake C, Cole SPC. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006, 86:849-899. 10.1152/physrev.00035.2005, 16816140.
72. Borst P, Evers R, Kool M, Wijnholds J. A family of drug transporters: The multidrug resistance-associated proteins. J Natl Canc Inst 2000, 92:1295-1302.
73. Ishikawa T. The ATP-dependent glutathione s-conjugate export pump. Trends Biochem Sci 1992, 17:463-469. 10.1016/0968-0004(92)90489-V, 1455517.
74. Sau A, Tregno FP, Valentino F, Federici G, Caccuri AM. Glutathione transferases and development of new principles to overcome drug resistance. Arch Biochem Biophys 2010, 500:116-122. 10.1016/j.abb.2010.05.012, 20494652.
75. Reddy BPN, Prasad GBKS, Raghavendra K. In silico analysis of glutathione S-transferase supergene family revealed hitherto unreported insect specific delta- and epsilon-GSTs and mammalian specific mu-GSTs in Ixodes scapularis (Acari: Ixodidae). Comput Biol Chem 2011, 35:114-120. 10.1016/j.compbiolchem.2011.03.004, 21514893.
76. 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 Biomembranes 2009, 1788:402-409.
77. Tarnay JN, Szeri F, Ilias A, Annilo T, Sung C, Le Saux O, Varadi A, Dean M, Boyd CD, 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. 10.1111/j.0962-1075.2004.00512.x, 15373810.
78. Chahine S, O'Donnell MJ. Physiological and molecular characterization of methotrexate transport by Malpighian tubules of adult Drosophila melanogaster. J Insect Physiol 2009, 55:927-935. 10.1016/j.jinsphys.2009.06.005, 19545574.
79. Chahine S, O'Donnell MJ. Interactions between detoxification mechanisms and excretion in Malpighian tubules of Drosophila melanogaster. J Exp Biol 2011, 214:462-468. 10.1242/jeb.048884, 21228205.
80. 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. 10.1093/nar/gkl606, 1635269, 16973896.
81. Huang H, Haddad GG. Drosophila dMRP4 regulates responsiveness to O-2 deprivation and development under hypoxia. Physiol Genomics 2007, 29:260-266. 10.1152/physiolgenomics.00166.2006, 17284667.
82. Monnier V, Girardot F, Cheret C, Andres O, Tricoire H. Modulation of oxidative stress resistance in Drosophila melanogaster by gene overexpression. Genesis 2002, 34:76-79. 10.1002/gene.10130, 12324953.
83. Campos I, Geiger JA, Santos AC, Carlos V, Jacinto A. Genetic screen in Drosophila melanogaster uncovers a novel set of genes required for embryonic epithelial repair. Genetics 2010, 184:129-U239. 10.1534/genetics.109.110288, 2815911, 19884309.
84. 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. 10.1002/ps.2218, 21681918.
85. Russel FGM, Koenderink JB, Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 2008, 29:200-207. 10.1016/j.tips.2008.01.006, 18353444.
86. Hopper-Borge E, Xu X, Shen T, Shi Z, Chen Z-S, Kruh GD. Human Multidrug Resistance Protein 7 (ABCC10) is a resistance factor for nucleoside analogues and epothilone B. Cancer Res 2009, 69:178-184. 10.1158/0008-5472.CAN-08-1420, 2745904, 19118001.
87. Waterhouse RM, Zdobnov EM, Tegenfeldt F, Li J, Kriventseva EV. OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Res 2011, 39:D283-D288. 10.1093/nar/gkq930, 3013786, 20972218.
88. Eleftherianos I, Won S, Chtarbanova S, Squiban B, Ocorr K, Bodmer R, Beutler B, Hoffmann JA, Imler J-L. ATP-sensitive potassium channel (K-ATP)-dependent regulation of cardiotropic viral infections. Proc Natl Acad Sci USA 2011, 108:12024-12029. 10.1073/pnas.1108926108, 3141999, 21719711.
89. Abo-Elghar GE, Fujiyoshi P, Matsumura F. Significance of the sulfonylurea receptor (SUR) as the target of diflubenzuron in chitin synthesis inhibition in Drosophila melanogaster and Blattella germanica. Insect Biochem Mol Biol 2004, 34:743-752. 10.1016/j.ibmb.2004.03.009, 15262279.
90. Gangishetti U, Breitenbach S, Zander M, Saheb SK, 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. 10.1016/j.ejcb.2008.09.002, 18996617.
91. Meyer F, Flötenmeyer M, Moussian B. The sulfonylurea receptor SUR is dispensable for chitin synthesis in Drosophila melanogaster embryos. Pest Manag Sci 2012, 10.1002/ps.3476.
92. Yoshiura K, Kinoshita A, Ishida T, Ninokata A, Ishikawa T, Kaname T, Bannai M, Tokunaga K, Sonoda S, Komaki R. A SNP in the ABCC11 gene is the determinant of human earwax type. Nat Genet 2006, 38:324-330. 10.1038/ng1733, 16444273.
93. Morita M, Imanaka T. Peroxisomal ABC transporters: Structure, function and role in disease. Biochim Biophys Acta Mol Basis Dis 1822, 2012:1387-1396.
94. Shani N, Sapag A, Valle D. Characterization and analysis of conserved motifs in a peroxisomal ATP-binding cassette transporter. J Biol Chem 1996, 271:8725-8730. 10.1074/jbc.271.15.8725, 8621506.
95. 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 USA 2011, 108:3228-3233. 10.1073/pnas.1015953108, 3044390, 21292982.
96. Zhou AM, Hassel BA, Silverman RH. Expression cloning of 2-5a-dependent RNAse - a uniquely regulated mediator of interferon action. Cell 1993, 72:753-765. 10.1016/0092-8674(93)90403-D, 7680958.
97. Paytubi S, Wang X, Lam YW, Izquierdo L, Hunter MJ, Jan E, Hundal HS, Proud CG. ABC50 promotes translation initiation in mammalian cells. J Biol Chem 2009, 284:24061-24073. 10.1074/jbc.M109.031625, 2782000, 19570978.
98. Kerr ID, Haider AJ, Gelissen IC. The ABCG family of membrane-associated transporters: you don't have to be big to be mighty. Br J Pharmacol 2011, 164:1767-1779. 10.1111/j.1476-5381.2010.01177.x, 3246702, 21175590.
99. Green MM. The ''genesis of the white-eyed mutant'' in Drosophila melanogaster: A reappraisal. Genetics 1996, 142:329-331. 1206968, 8852833.
100. Mills LR. Structure of visual system of 2-spotted spider-mite, Tetranychus urticae. J Insect Physiol 1974, 20:795-808. 10.1016/0022-1910(74)90171-1, 4840682.
101. Zhang SD, Odenwald WF. Misexpression of the white (omega) gene triggers male-made courtship in Drosophila. Proc Natl Acad Sci USA 1995, 92:5525-5529. 10.1073/pnas.92.12.5525, 41728, 7777542.
102. Anaka M, MacDonald CD, Barkova E, Simon K, Rostom R, Godoy RA, Haigh AJ, Meinertzhagen IA, Lloyd V. The white gene of Drosophila melanogaster encodes a protein with a role in courtship behavior. J Neurogenet 2008, 22:243-276. 10.1080/01677060802309629, 19012054.
103. Borycz J, Borycz JA, Kubow A, Lloyd V, Meinertzhagen IA. 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. 10.1242/jeb.021162, 18931318.
104. 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. 10.1111/j.1365-2443.2011.01490.x, 21294818.
105. McQuilton P, St Pierre SE, Thurmond J, FlyBase C. FlyBase 101-the basics of navigating FlyBase. Nucleic Acids Res 2012, 40:D706-D714. 10.1093/nar/gkr1030, 3245098, 22127867.
106. wFleaBase - Daphnia Water Flea Genome Database http://wfleabase.org/.
107. Graf GA, Yu LQ, Li WP, Gerard R, Tuma PL, Cohen JC, Hobbs HH. ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion. J Biol Chem 2003, 278:48275-48282. 10.1074/jbc.M310223200, 14504269.
108. 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 USA 2000, 97:9519-9524. 10.1073/pnas.160271797, 16897, 10931948.
109. Itoh TQ, Tanimura T, Matsumoto A. Membrane-bound transporter controls the circadian transcription of clock genes in Drosophila. Genes Cells 2011, 16:1159-1167. 10.1111/j.1365-2443.2011.01559.x, 22077638.
110. Kuwana H, ShimizuNishikawa K, Iwahana H, Yamamoto D. Molecular cloning and characterization of the ABC transporter expressed in Trachea (ATET) gene from Drosophila melanogaster. Biochim Biophys Acta Gene Struct Expr 1996, 1309:47-52.
111. Jones CM, Toé HK, Sanou A, Namountougou M, Hughes A. Additional selection for insecticide resistance in urban malaria vectors: DDT Resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS One 2012, 7:e45995. 10.1371/journal.pone.0045995, 3457957, 23049917.
112. Lamping E, Baret PV, Holmes AR, Monk BC, Goffeau A, Cannon RD. Fungal PDR transporters: Phylogeny, topology, motifs and function. Fungal Genet Biol 2010, 47:127-142. 10.1016/j.fgb.2009.10.007, 2814995, 19857594.
113. Robinson SW, Herzyk P, Dow JAT, Leader DP. FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic Acids Res 2013, 41:D744-D750. 10.1093/nar/gks1141, 3531048, 23203866.
114. Mummery-Widmer JL, Yamazaki M, Stoeger T, Novatchkova M, Bhalerao S, Chen D, Dietzl G, Dickson BJ, Knoblich JA. Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 2009, 458:987-U959. 10.1038/nature07936, 2988197, 19363474.
115. Zhang S, Feany MB, Saraswati S, Littleton JT, 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. 10.1242/dmm.000653, 2675792, 19380309.
116. Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK. Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 2005, 14:607-613. 10.1111/j.1365-2583.2005.00589.x, 16313561.
117. Diamond back moth Genome database http://iae.fafu.edu.cn/DBM.
118. Zhao ZY, Sheps JA, Ling V, Fang LL, Baillie DL. Expression analysis of ABC transporters reveals differential functions of tandemly duplicated genes in Caenorhabditis elegans. J Mol Biol 2004, 344:409-417. 10.1016/j.jmb.2004.09.052, 15522294.
119. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
120. ORCAE. Online Resource for Communnity Annotation of Eukaryots http://bioinformatics.psb.ugent.be/orcae/overview/Tetur.
121. ScanProsite tool http://prosite.expasy.org/scanprosite.
122. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
123. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263, 15647292.
124. Jobb G, Von Haeseler A, Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 2004, 4:18. 10.1186/1471-2148-4-18, 459214, 15222900.
125. Allikmets R, Gerrard B, Hutchinson A, Dean M. Characterization of the human ABC superfamily: Isolation and mapping of 21 new genes using the expressed sequence tags database. Hum Mol Genet 1996, 5:1649-1655. 10.1093/hmg/5.10.1649, 8894702.
126. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 2011, 28:2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
127. Campanella JJ, Bitincka L, Smalley J. MatGAT: An application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinforma 2003, 4:29.
128. Bernsel A, Viklund H, Falk J, Lindahl E, Von Heijne G, Elofsson A. Prediction of membrane-protein topology from first principles. Proc Natl Acad Sci USA 2008, 105:7177-7181. 10.1073/pnas.0711151105, 2438223, 18477697.
129. 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. 10.1038/nprot.2007.131, 17446895.
130. Rambaldi D, Ciccarelli FD. FancyGene: dynamic visualization of gene structures and protein domain architectures on genomic loci. Bioinformatics 2009, 25:2281-2282. 10.1093/bioinformatics/btp381, 2734320, 19542150.
131. NetNGlyc server 1.0 http://www.cbs.dtu.dk/services/NetNGlyc/.
132. Julenius K, Molgaard A, Gupta R, Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 2005, 15:153-164.
133. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106. 10.1186/gb-2010-11-10-r106, 3218662, 20979621.