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 Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Xiong, Jie ^a,d   Feng, Lifang ^a,c,d   Yuan, Dongxia ^a   Fu, Chengjie ^a,b   Miao, Wei ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UPPSALA UNIVERSITY   (Sweden)

^c ZHEJIANG GONGSHANG UNIVERSITY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; CILIATE; DIVERGENCE; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; HYDROLYSIS; PHYLOGENETICS; TAXONOMY; TOPOLOGY; TOXICOLOGY;

CILIOPHORA; EUKARYOTA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

ABC TRANSPORTER;

ARTICLE; GENETICS; MOLECULAR EVOLUTION; MULTIGENE FAMILY; TETRAHYMENA THERMOPHILA;

ATP-BINDING CASSETTE TRANSPORTERS; EVOLUTION, MOLECULAR; MULTIGENE FAMILY; TETRAHYMENA THERMOPHILA;

EID: 77958458748     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-330     Document Type: Article

References (81)

1. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules organisms from bacteria to humans. IB Holland MA Blight, J Mol Biol 1999 293 2 381 399 10.1006/jmbi.1999.2993 10529352
2. Structure and mechanism of ABC transporter proteins. K Hollenstein RJP Dawson KP Locher, Curr Opin Struc Biol 2007 17 4 412 418 10.1016/j.sbi.2007.07. 003 (Pubitemid 47451766)
3. The ATP-binding cassette family: a structural perspective. V Kos RC Ford, Cellular and Molecular Life Sciences 2009 66 19 3111 3126 10.1007/s00018-009- 0064-9 19544044
4. An inventory of the human ABC proteins. I Klein B Sarkadi A Varadi, Biochim Biophys Acta 1999 1461 2 237 262 10.1016/S0005-2736(99)00161-3 10581359
5. The human ATP-binding cassette (ABC) transporter superfamily. M Dean Y Hamon G Chimini, Journal of Lipid Research 2001 42 7 1007 1017 11441126 (Pubitemid 32645780)
6. Overview: ABC transporters and human disease. MM Gottesman SV Ambudkar, Journal of Bioenergetics and Biomembranes 2001 33 6 453 458 10.1023/A: 1012866803188 11804186
7. Multidrug resistance in cancer: Role of ATP-dependent transporters. MM Gottesman T Fojo SE Bates, Nature Reviews Cancer 2002 2 1 48 58 10.1038/nrc706 11902585
8. Multidrug resistance in parasites: ABC transporters, P-glycoproteins and molecular modelling. PM Jones AM George, International Journal for Parasitology 2005 35 5 555 566 10.1016/j.ijpara.2005.01.012 15826647
9. Tobacco budworm P-glycoprotein: Biochemical characterization and its involvement in pesticide resistance. CL Lanning RL Fine JJ Corcoran HM Ayad RL Rose MB AbouDonia, Biochimica Et Biophysica Acta-General Subjects 1996 1291 2 155 162 10.1016/0304-4165(96)00060-8 (Pubitemid 26348769)
10. Stimulatory effect of insecticides on partially purified P-glycoprotein ATPase from the resistant pest Helicoverpa armigera. R Aurade SK Jayalakshmi K Sreeramulu, Biochemistry and Cell Biology-Biochimie Et Biologie Cellulaire 2006 84 6 1045 1050 10.1139/O06-194 17215890
11. Effect of insecticides on P-glycoprotein ATPase activity of the insecticide resistant pest Helicoverpa armigera. K Sreeramulu R Srinivas SK Jayalakshmi, Biochemistry and Cell Biology-Biochimie Et Biologie Cellulaire 2006 84 6 1059 1060
12. The pharmacology of cancer resistance. R O'Connor, Anticancer Research 2007 27 3A 1267 1272 17593618
13. Drug Transporters: Recent Advances and Therapeutic Applications. RM Franke A Sparreboom, Clinical Pharmacology & Therapeutics 2010 87 1 3 7
14. Involvement of ABC transporters in pharmacokinetics and toxicokinetics. D Kroetz, Toxicology Letters 2009 189 17 S17 10.1016/j.toxlet.2009.06.009
15. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. M Dean T Annilo, Annual Review of Genomics and Human Genetics 2005 6 123 142 10.1146/annurev.genom.6.080604.162122 16124856
16. Identification of the Anopheles gambiae ATP-binding cassette transporter superfamily genes. CW Roth I Holm M Graille P Dehoux A Rzhetsky P Wincker J Weissenbach PT Brey, Molecules and Cells 2003 15 2 150 158 12803476
17. The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. JA Sheps S Ralph ZY Zhao DL Baillie V Ling, Genome Biology 2004 5 3 15 10.1186/gb-2004-5-3-r15 15003118
18. Yeast ABC transporters - A tale of sex, stress, drugs and aging. H Jungwirth K Kuchler, Febs Letters 2006 580 4 1131 1138 10.1016/j.febslet.2005. 12.050 16406363
19. ATP-binding cassette transporters in Escherichia coli. A Moussatova C Kandt ML O'Mara DP Tieleman, Biochimica Et Biophysica Acta-Biomembranes 2008 1778 9 1757 1771 10.1016/j.bbamem.2008.06.009
20. The Escherichia coli ATP-binding cassette (ABC) proteins. KJ Linton CF Higgins, Molecular Microbiology 1998 28 1 5 13 10.1046/j.1365-2958.1998.00764.x 9593292
21. ATP-binding cassette transporters in bacteria. AL Davidson J Chen, Annual Review of Biochemistry 2004 73 241 268 10.1146/annurev.biochem.73.011303.073626 15189142
22. Structure, function, and evolution of bacterial ATP-binding cassette systems. AL Davidson E Dassa C Orelle J Chen, Microbiology and Molecular Biology Reviews 2008 72 2 317 364 10.1128/MMBR.00031-07 18535149
23. ABC transporters in the protozoan parasite Leishmania. JM Perez-Victoria A Parodi-Talice C Torres F Gamarro S Castanys, Int Microbiol 2001 4 3 159 166 11820434
24. ABC transporters and drug resistance in parasitic protozoa. A Klokouzas S Shahi SB Hladky MA Barrand HW van Veen, International Journal of Antimicrobial Agents 2003 22 3 301 317 10.1016/S0924-8579(03)00210-3 13678838
25. Tetrahymena thermophila. K Collins MA Gorovsky, Current Biology 2005 15 9 317 R318 10.1016/j.cub.2005.04.039 15886083
26. Analysis of expressed sequence tags (ESTs) in the ciliated protozoan Tetrahymena thermophila. JS Fillingham ND Chilcoat AP Turkewitz E Orias M Reith RE Pearlman, Journal of Eukaryotic Microbiology 2002 49 2 99 107 10.1111/j.1550-7408.2002.tb00350.x 12043965
27. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. JA Eisen RS Coyne M Wu DY Wu M Thiagarajan JR Wortman JH Badger QH Ren P Amedeo KM Jones,, et al. Plos Biology 2006 4 9 1620 1642 10.1371/journal.pbio.0040286 (Pubitemid 44379925)
28. Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. W Miao J Xiong J Bowen W Wang Y Liu O Braguinets J Grigull RE Pearlman E Orias MA Gorovsky, PLoS ONE 2009 4 2 4429 10.1371/journal.pone. 0004429 19204800
29. Tetrahymena Genome Database (TGD): a new genomic resource for Tetrahymena thermophila research. NA Stover CJ Krieger G Binkley Q Dong DG Fisk R Nash A Sethuraman S Weng JM Cherry, Nucleic Acids Research 2006 34 Database 500 503 10.1093/nar/gkj054 16381920
30. Genome-wide identification and characterization of cytochrome P450 monooxygenase genes in the ciliate Tetrahymena thermophila. CJ Fu J Xiong W Miao, Bmc Genomics 2009 10 208 10.1186/1471-2164-10-208 19409101
31. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. R Sanchez-Fernandez TGE Davies JOD Coleman PA Rea, Journal of Biological Chemistry 2001 276 32 30231 30244 10.1074/jbc.M103104200 11346655
32. Evolutionary analyses of ABC transporters of Dictyostelium discoideum. C Anjard WF Loomis, Eukaryotic Cell 2002 1 4 643 652 10.1128/EC.1.4.643-652.2002 12456012
33. Evolution of gene families: the multidrug resistance transporter genes in five related yeast species. Y Gbelska JJ Krijger KD Breunig, Fems Yeast Research 2006 6 3 345 355 10.1111/j.1567-1364.2006.00058.x 16630275
34. An ATP-binding cassette transporter is a major glycoprotein of sea urchin sperm membranes. KJ Mengerink VD Vacquier, Journal of Biological Chemistry 2002 277 43 40729 40734 10.1074/jbc.M207184200 12193601
35. Cell division induced by mechanical stimulation in starved Tetrahymena thermophila: cell cycle without synthesis of macronuclear DNA. M Iwamoto T Sugai Y Nakaoka, Cell Biology International 2004 28 7 503 509 10.1016/j.cellbi.2004. 04.004 15261157
36. Identification of a human mitochondrial ABC transporter, the functional orthologue of yeast Atm1p. P Csere R Lill G Kispal, FEBS Letters 1998 441 2 266 270 10.1016/S0014-5793(98)01560-9 9883897
37. MTABC3, a novel mitochondrial ATP-binding cassette protein involved in iron homeostasis. N Mitsuhashi T Miki H Senbongi N Yokoi H Yano M Miyazaki N Nakajima T Iwanaga Y Yokoyama T Shibata,, et al. Journal of Biological Chemistry 2000 275 23 17536 17540 10.1074/jbc.275.23.17536 10837493
38. Multidrug resistance: Retrospect and prospects in anti-cancer drug treatment. R Perez-Tomas, Current Medicinal Chemistry 2006 13 16 1859 1876 10.2174/092986706777585077 16842198
39. The Yeast Ste6 Gene Encodes a Homolog of the Mammalian Multidrug Resistance P-Glycoprotein. JP Mcgrath A Varshavsky, Nature 1989 340 6232 400 404 10.1038/340400a0 2569166
40. Uptake and efflux of polycyclic aromatic hydrocarbons by Tetrahymena pyriformis: Evidence for a resistance mechanism. M Bamdad S Reader CA Groliere J Bohatier F Denizeau, Cytometry 1997 28 2 170 175 10.1002/(SICI)1097- 0320(19970601)28:2<170::AID-CYTO11>3.0.CO;2-N 9181308
41. Identification of a multidrug resistance-like system in Tetrahymena pyriformis: evidence for a new detoxication mechanism in freshwater ciliates. M Bamdad P Brousseau F Denizeau, Febs Letters 1999 456 3 389 393 10.1016/S0014-5793(99)00978-3 10462050
42. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. EM Leslie RG Deeley SPC Cole, Toxicology and Applied Pharmacology 2005 204 3 216 237 10.1016/j.taap.2004.10.012 15845415
43. Glutathione S-transferase M1 and multidrug resistance protein 1 Act in synergy to protect melanoma cells from vincristine effects. P Depeille P Cuq S Mary I Passagne A Evrard D Cupissol L Vian, Molecular Pharmacology 2004 65 4 897 905 10.1124/mol.65.4.897 15044619
44. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta-oxidation. BK Zolman ID Silva B Bartel, Plant Physiology 2001 127 3 1266 1278 10.1104/pp.010550 11706205
45. Import of proteins into peroxisomes. EH Hettema B Distel HF Tabak, Bba-Mol Cell Res 1999 1451 1 17 34
46. A Saccharomyces cerevisiae homolog of the human adrenoleukodystrophy transporter is a heterodimer of two half ATP-binding cassette transporters. N Shani D Valle, Proceedings of the National Academy of Sciences of the United States of America 1996 93 21 11901 11906 10.1073/pnas.93.21.11901 8876235
47. The human ATP-binding cassette (ABC) transporter superfamily. M Dean A Rzhetsky R Allikmets, Genome Res 2001 11 7 1156 1166 10.1101/gr.GR-1649R 11435397 (Pubitemid 32677289)
48. The human peroxisomal ABC half transporter ALDP functions as a homodimer and accepts acyl-CoA esters. CWT van Roermund WF Visser L Ijlst A van Cruchten M Boek W Kulik HR Waterham RJA Wanders, Faseb Journal 2008 22 12 4201 4208 10.1096/fj.08-110866 18757502
49. Cloning and Characterization of a Rnase-L Inhibitor - a New Component of the Interferon-Regulated 2-5a Pathway. C Bisbal C Martinand M Silhol B Lebleu T Salehzada, Journal of Biological Chemistry 1995 270 22 13308 13317 10.1074/jbc.270.22.13308 7539425
50. Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2 alpha kinase GCN2. MJ Marton CRV deAldana HF Qiu K Chakraburtty AG Hinnebusch, Mol Cell Biol 1997 17 8 4474 4489 9234705
51. Dominant-negative inhibition of breast cancer resistance protein as drug efflux pump through the inhibition of S-S dependent homodimerization. K Kage S Tsukahara T Sugiyama S Asada E Ishikawa T Tsuruo Y Sugimoto, International Journal of Cancer 2002 97 5 626 630 10.1002/ijc.10100 (Pubitemid 34087801)
52. Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. JK Xu Y Liu YY Yang S Bates JT Zhang, Journal of Biological Chemistry 2004 279 19 19781 19789 10.1074/jbc.M310785200 15001581
53. ABCdb: an ABC transporter database. Y Quentin G Fichant, J Mol Microb Biotech 2000 2 4 501 504
54. A comparative analysis of ABC transporters in complete microbial genomes. K Tomii M Kanehisa, Genome Res 1998 8 10 1048 1059 9799792
55. Getting in or out: Early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. W Saurin M Hofnung E Dassa, J Mol Evol 1999 48 1 22 41 10.1007/PL00006442 9873074
56. Structure, function and evolution of multidomain proteins. C Vogel M Bashton ND Kerrison C Chothia SA Teichmann, Curr Opin Struc Biol 2004 14 2 208 216 10.1016/j.sbi.2004.03.011 (Pubitemid 38490788)
57. Inventory and comparative analysis of rice Arabidopsis ATP-binding cassette (ABC) systems. O Garcia P Bouige C Forestier E Dassa, J Mol Biol 2004 343 1 249 265 10.1016/j.jmb.2004.07.093 15381434
58. ABC transporter architecture and regulatory roles of accessory domains. E Biemans-Oldehinkel MK Doeven B Poolman, FEBS Letters 2006 580 4 1023 1035 10.1016/j.febslet.2005.11.079 16375896
59. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. PC Smith N Karpowich L Millen JE Moody J Rosen PJ Thomas JF Hunt, Mol Cell 2002 10 1 139 149 10.1016/S1097-2765(02)00576-2 12150914
60. The evolution of spliceosomal Introns in alveolates. HD Nguyen M Yoshihama N Kenmochi, Molecular Biology and Evolution 2007 24 5 1093 1096 10.1093/molbev/msm037 17331959
61. Genome architecture drives protein evolution in ciliates. RA Zufall CL McGrath SV Muse LA Katz, Molecular Biology and Evolution 2006 23 9 1681 1687 10.1093/molbev/msl032 16760419
62. The evolutionary fate and consequences of duplicate genes. M Lynch JS Conery, Science 2000 290 5494 1151 1155 10.1126/science.290.5494.1151 11073452
63. Functional diversification of duplicate genes through subcellular adaptation of encoded proteins. AC Marques N Vinckenbosh D Brawand H Kaessmann, Genome Biology 2008 9 3 54 10.1186/gb-2008-9-3-r54 18336717
64. The evolution of gene duplications: classifying and distinguishing between models. H Innan F Kondrashov, Nature Reviews Genetics 2010 11 2 97 108 20051986
65. Statistical framework for phylogenomic analysis of gene family expression profiles. X Gu, Genetics 2004 167 1 531 542 10.1534/genetics.167.1.531 15166175
66. Comparative methods for the analysis of gene-expression evolution: An example using yeast functional genomic data. TH Oakley ZL Gu E Abouheif NH Patel WH Li, Molecular Biology and Evolution 2005 22 1 40 50 10.1093/molbev/msh257 15356281
67. The probability of duplicate gene preservation by subfunctionalization. M Lynch A Force, Genetics 2000 154 1 459 473 10629003
68. The pattern of evolution of smaller-scale gene duplicates in mammalian genomes is more consistent with neo-than subfunctionalisation. T Hughes DA Liberles, J Mol Evol 2007 65 5 574 588 10.1007/s00239-007-9041-9 17957399
69. Selection in the evolution of gene duplications. FA Kondrashov IB Rogozin YI Wolf EV Koonin, Genome Biology 2002 3 2 ESEARCH0008 10.1186/gb-2002-3-2- research0008 11864370
70. Gene dosage balance: deletions, duplications and dominance. RA Veitia, Trends Genet 2005 21 1 33 35 10.1016/j.tig.2004.11.002 15680512
71. Functional partitioning of yeast co-expression networks after genome duplication. GC Conant KH Wolfe, Plos Biology 2006 4 4 545 554 10.1371/journal.pbio.0040109
72. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. S Capella-Gutierrez JM Silla-Martinez T Gabaldon, Bioinformatics 2009 25 15 1972 1973 10.1093/bioinformatics/btp348 19505945
73. PhyML: Fast and Accurate Phylogeny Reconstruction by Maximum Likelihood. S Guindon JF Dufayard W Hordijk V Lefort O Gascuel, Infection Genetics and Evolution 2009 9 3 384 385
74. Tetrahymena as a laboratory organism: Useful strains, cell culture, and cell line maintenance. E Orias EP Hamilton JD Orias, Methods in Cell Biology, Vol 62 2000 62 189 211 full-text
75. Identification of differentially expressed genes in Tetrahmena thermophila in response to dichlorodiphenyltrichloroethane (DDT) by suppression subtractive hybridization. W Miao T Yu E Orias ML Wan CJ Fu, Environmental Microbiology 2006 8 6 1122 1129 10.1111/j.1462-2920.2006.00988.x 16689733
76. Difterentially expressed genes of Tetrahymena thermophila in response to tributyltin (TBT) identified by suppression subtractive hybridization and real time quantitative PCR. LF Feng W Miao YX Wu, Aquatic Toxicology 2007 81 1 99 105 10.1016/j.aquatox.2006.11.005 17188762
77. MODELTEST: testing the model of DNA substitution. D Posada KA Crandall, Bioinformatics 1998 14 9 817 818 10.1093/bioinformatics/14.9.817 9918953
78. PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0 Beta. DL Swofford, Sinauer Associates, Sunderland, Mass 2001
79. CoMET: A Mesquite package for comparing models of continuous character evolution on phylogenies. C Lee S Blay AO Mooers A Singh TH Oakley, Evol Bioinform Online 2006 2 183 186
80. Mesquite: a modular system for evolutionary analysis. Version 2.5. DM WP Maddison, 2008 http://mesquiteproject.org
81. PAML: a program package for phylogenetic analysis by maximum likelihood. ZH Yang, Computer Applications in the Biosciences 1997 13 5 555 556 9367129