Background: ATP-binding cassette (ABC) transporters are transmembrane proteins that utilize the energy of adenosine triphosphate (ATP) binding and hydrolysis to transport various substrates across extra and intracellular membranes, including metabolic products, lipids and sterols, and drugs. They play important roles in various processes of life, especially in drug resistance, metabolism and development. Objective: Identify the ATP-binding cassette (ABC) transporter gene family and their members in the genome of silkworm, Bombyx mori. Method: Bioinformatics and phylogenetic analysis were used in the study. Results: We identified 47 ABC proteins in the silkworm genome, which possesses members of all current ABC subfamilies A to H. ABC proteins of silkworm were compared to those from worm, fruit fly and human. A high conservation of silkworm ABC transporters were observed for proteins involved in fundamental cellular processes, including the half transporters of the ABCB subfamily, which function in iron metabolism and transport of Fe/S protein precursors, and the members of subfamilies ABCD, ABCE and ABCF, which have roles in very long chain fatty acid transport. Both ABCE and F gene products may be involved in an innate immune response to viral infections. As in the fly, ABCH proteins are inverse half-transporters showing the same domain architecture as the members of the ABCG subfamily, and ABCG transporters involve in transportation of ommochrome precursors and uric acid into pigment granules and urate granules. Conclusion: These results paved the way for further study on the function of the ABC transporters in silkworm, Bombyx mori.
Published in | American Journal of Bioscience and Bioengineering (Volume 3, Issue 5) |
DOI | 10.11648/j.bio.20150305.27 |
Page(s) | 123-133 |
Creative Commons |
This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited. |
Copyright |
Copyright © The Author(s), 2015. Published by Science Publishing Group |
ATP-binding Cassette Transporters, Silkworm, ABCG, Cholesterol Efflux, Multidrug Resistance-associated Protein, Insect
[1] | Holland IB. ABC transporters, mechanisms and biology: an overview. Essays Biochem. 2011 Sep 7; 50(1): 1-17. |
[2] | Wilkens S. Structure and mechanism of ABC transporters. F1000Prime Rep. 2015 Feb 3; 7: 14. |
[3] | Dassa E, Bouige P. The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 2001, 152: 211-229. |
[4] | Dean M, Hamon Y, Chimini G. The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 2001, 42: 1007-1017. |
[5] | Hollenstein K, Frei DC, Locher KP. Structure of an ABC transporter in complex with its binding protein. Nature 2007, 446: 213-216. |
[6] | Dawson RJ, Locher KP. Structure of a bacterial multidrug ABC transporter. Nature 2006, 443: 180-185. |
[7] | Klein I, Sarkadi B, Váradi A. An inventory of the human ABC proteins. Biochim Biophys Acta 1999, 1461: 237-262. |
[8] | Dean M., Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 2001, 11: 1156-1166. |
[9] | Annilo T, Chen ZQ, Shulenin S, et al. Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics 2006, 88: 1-11. |
[10] | Dean M, Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 2005, 6: 123-142. |
[11] | Wu ZB, Wu JM. The G subfamily of ATP-binding cassette (ABC) transporters and human diseases. Journal of Jiangsu University (Medicine Edition) 2008, 18(3): 861–866. |
[12] | Gottesman MM, Ambudkar SV. Overview: ABC transporters and human disease. Bioenerg Biomembr 2001, 33: 453-458. |
[13] | Li G, Gu HM, Zhang DW. ATP-binding cassette transporters and cholesterol translocation. IUBMB Life. 2013 Jun; 65(6): 505-12. |
[14] | Hlaváč V, Souček P. Role of family D ATP-binding cassette transporters (ABCD) in cancer. Biochem Soc Trans. 2015 Oct 1; 43(5): 937-42. |
[15] | Ween MP, Armstrong MA, Oehler MK, Ricciardelli C. The role of ABC transporters in ovarian cancer progression and chemoresistance. Crit Rev Oncol Hematol. 2015 Nov; 96(2): 220-56. |
[16] | Gatti L, Cossa G, Beretta GL, Zaffaroni N, Perego P. Novel insights into targeting ATP-binding cassette transporters for antitumor therapy. Curr Med Chem. 2011; 18(27): 4237-49. |
[17] | Bloise E, Ortiga-Carvalho TM, Reis FM, Lye SJ, Gibb W, Matthews SG. ATP-binding cassette transporters in reproduction: a new frontier. Hum Reprod Update. 2015 Nov 5. pii: dmv049. [Epub ahead of print] |
[18] | Ling, V, Kartner, N, Sudo, T, et al. Multidrug-resistance phenotype in Chinese hamster ovary cells. Cancer Treat Rep 1983, 67, 869−874. |
[19] | Gottesman, MM. Drug-resistant mutants: selection and dominance analysis. Methods Enzymol 1987, 151: 113−121. |
[20] | Riordan JR, Ling V. Purification of P-glycoprotein from plasma membrane vesicles of chinese hamster ovary cell mutants with reduced colchicine permeability. Biol Chem 1979, 254: 12701-12705. |
[21] | Gerlach JH, Endicott JA, Juranka PF, et al. Homology between P-glycoprotein and a bacterial heamolysin transport protein suggests a model for multidrug resistance. Nature 1986, 324: 485-489. |
[22] | Cole SP, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258: 1650-1654. |
[23] | Doyle LA, Yang W, Abruzzo LV, et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 1998, 95: 15665-15670. |
[24] | Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat Rev Cancer 2002, 2: 48-58. |
[25] | Bodo A, Bakos E, Szeri F, et al. The role of multid-drug transporters in drug availability, metabolism and toxicity. Toxicol Lett 2003, 140-141: 133-143. |
[26] | Xia et al. [http://silkworm.genomics.org.cn/]. |
[27] | Kerr ID. Structure and association of ATP-binding cassette transporter nucleotide-binding domains. Biochim Biophys Acta 2002, 1561: 47-64. |
[28] | ExPASy (Expert Protein Analysis System) proteomics server of the Swiss Institute of Bioinformatics (SIB), Scan Prosite facility [http://expasy.org/tools/scanprosite/]. |
[29] | Peelman F, Labeur C, Vanloo B, et al. Characterization of the ABCA transporter subfamily: identification of prokaryotic and eukaryotic members, phylogeny and topology. Mol Biol 2003, 325: 259-274. |
[30] | Kubo Y, Sekiya S, Ohigashi M, et al. ABCA5 resides in lysosomes, and ABCA5 knockout mice develop lysosomal disease-like symptoms. Mol Cell Biol 2005, 25: 4138–4149. |
[31] | Albrecht C, Viturro E.The ABCA subfamily gene and protein structures, functions and associated hereditary diseases [J]. Pflugers Arch - Eur J Physiol 2007, 453: 581–589. |
[32] | Kaminski WE, Wenzel JJ, Piehler A, et al. ABCA6, a novel a subclass ABC transporter. Biochem Biophys Res Commun 2001, 285: 1295–1301. |
[33] | Akiyama M, Sugiyama-Nakagiri Y, Sakai K, et al. Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. Clin Invest 2005, 115: 1777–1784. |
[34] | Prades C, Arnould I, Annilo T, et al. The human ATP binding cassette gene ABCA13, located on chromosome 7p12.3, encodes a 5058 amino acid protein with an extracellular domain encoded in part by a 4.8-kb conserved exon. Cytogenet Genome Res 2002, 98: 160–168. |
[35] | Wenzel JJ, Piehler A, Kaminski WE. ABCA subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport. Front Biosci 2007, 12: 3177-3193. |
[36] | Schinkel AH, Mol CA, Wagenaar E, et al. Multidrug resistance and the role of P-glycoprotein knockout mice. Eur Cancer 1995, 31A, 1295-1298. |
[37] | Wu CT, Budding M, Griffin MS, et al. Isolation and characterization of Drosophila multidrug resistance gene homologs. Mol Cell Biol 1991, 11: 3940-3948. |
[38] | Gerrard B, Stewart C, Dean M. Analysis of Mdr50: A Drosophila P-glycoprotein/multidrug resistance gene homolog. Genomics 1993, 17: 83-88. |
[39] | Begun DJ, Whitley P. Genetics of alpha-amanitin resistance in a natural population of Drosophila melanogaster. Heredity 2000, 85(Pt2): 184-190. |
[40] | Tapadia MG, Lakhotia SC. 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. |
[41] | Vache C, Camares O, Cardoso-Ferreira MC, et al. A potential genomic biomarker for the detection of polycyclic aromatic hydrocarbon pollutants: multidrug resistance gene 49 in Drosophila melanogaster. Environ Toxicol Chem 2007, 26: 1418-1424. |
[42] | Abele R, Tampe R. Modulation of the antigen transport machinery TAP by friends and enemies. FEBS Lett 2006, 580: 1156-1163. |
[43] | Herget M, Tampe R. Intracellular peptide transporters in human compartmentalization of the "peptidome". Pflugers Arch 2007, 453: 591-600. |
[44] | Zhang F, Zhang W, Liu L, et al. Characterization of ABCB9, an ATP binding cassette protein associated with lysosomes. Biol Chem 2000, 275: 23287-23294. |
[45] | Sturm A, Cunningham P, Dean M. The ABC transporter gene family of Daphnia pulex. BMC Genomics 2009, 10: 170. |
[46] | Aleksandrov AA, Aleksandrov LA, Riordan JR. CFTR (ABCC7) is a hydrolyzable-ligand-gated channel. Pflugers Arch 2007, 453: 693-702. |
[47] | Moreau C, Prost AL, Derand R, et al. SUR, ABC proteins targeted by KATP channel openers. Mol Cell Cardiol 2005, 38: 951-963. |
[48] | Kruh GD, Belinsky MG. The MRP family of drug efflux pumps [J].Oncogene 2003, 22: 7537-7552. |
[49] | Conti LR, Radeke CM, Shyng SL, et al. Transmembrane topology of the sulfonylurea receptor SUR1. Biol Chem 2001, 276: 41270-41278. |
[50] | Deeley RG, Westlake C, Cole SP. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006, 86: 849-899. |
[51] | Akasaka T,Klinedinst S, Ocorr K,et al. The ATP-sensitive potassium (KATP) channel-encoded dSUR gene is required for Drosophila heart function and is regulated by tinman. Proc Natl Acad Sci USA 2006, 103: 11999-12004. |
[52] | Nasonkin I, Alikasifoglu A, Ambros e C, et al.A novel sulfonylurea receptor amily member expressed in the embryonic Drosophila dorsal vessel and tracheal system. Biol Chem 1999, 274: 29420-29425. |
[53] | Tarnay JN, Szeri F, Ilias A, et al. 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. |
[54] | Grailles M, Brey PT, Roth CW. The Drosophila melanogaster multidrug-resistance protein 1 (MRP1) homolog has a novel gene structure containing two variable internal exons. Gene 2003, 307: 41-50. |
[55] | Kruh GD, Guo Y, Hopper-Borge E, et al. ABCC10, ABCC11, and ABCC12. Pflugers Arch 2007, 453: 675-684. |
[56] | Rubin GM, Yandell MD, Wortman JR, et al. Comparative genomics of the eukaryotes. Science 2000, 287: 2204-2215. |
[57] | Harrison PM, Echols N, Gerstein MB. Digging for dead genes: an analysis of the characteristics of the pseudogene population in the Caenorhabditis elegans genome. Nucleic Acids Res 2001, 29: 818-830. |
[58] | Mounsey A, Bauer P, Hope IA.Evidence suggesting that a fifth of annotated Caenorhabditis elegans genes may be pseudogenes. Genome Res, 2002, 12: 770-775. |
[59] | Theodoulou FL, Holdsworth M, Baker A: Peroxisomal ABC transporters. FEBS Lett 2006, 580: 1139-1155. |
[60] | Petriv OI, Pilgrim DB, Rachubinski RA, et al. RNA interference of peroxisome-related genes in C. elegans: a new model for human peroxisomal disorders. Physiol Genomics 2002, 10: 79-91. |
[61] | Berger J, Gartner J. X-linked adrenoleukodystrophy: clinical, biochemical and pathogenetic aspects. Biochim Biophys Acta 2006, 1763: 1721-1732. |
[62] | Kerr ID. Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Commun 2004, 315: 166-173. |
[63] | Allikmets R, Schriml LM, Hutchinson A, et al. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res 1998, 58, 5337−5339. |
[64] | Zhou A, Hassel BA, Silverman RH. Expression cloning of 2-5Adependent RNAase: a uniquely regulated mediator of interferon action. Cell 1993, 72: 753-765. |
[65] | Chen ZQ, Dong J, Ishimura A, et al. The essential vertebrate ABCE1 protein interacts with eukaryotic initiation factors. Biol Chem 2006, 281: 7452-7457. |
[66] | Marton MJ, Vazquez de Aldana CR, Qiu H. Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2alpha kinase GCN2. Mol Cell Biol 1997, 17, 4474−4489. |
[67] | Tyzack JK, Wang X., Belsham GJ, et al. ABC50 interacts with eukaryotic initiation factor 2 and associates with the ribosome in an ATP-dependent manner. Biol Chem 2000, 275, 34131-34139. |
[68] | Savary S, Denizot F. Luciani M, et al. Molecular cloning of a mammalian ABC transporter homologous to Drosophila white gene, Mamm Genome 1996, 7: 673-676. |
[69] | Dreesen TD, Johnson DH, Henikoff S. The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol Cell Biol 1988, 8: 5206-5215. |
[70] | Sullivan DT, Bell LA, Paton DR, et al. Purine transport by malpighian tubules of pteridine-deficient eye color mutants of Drosophila melanogaster. Biochem Genet 1979, 17: 565-573. |
[71] | Tearle RG, Belote JM, McKeown M, et al. Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics 1989, 122: 595–606. |
[72] | Crouzet J, Trombik T, Fraysse AS, et al. Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett 2006, 580: 1123-1130. |
[73] | Paul T. Tarra, Elizabeth J. Tarling, Dragana D. Bojanic, et al. Emerging new paradigms for ABCG transporters. Biochimica et Biophysica Acta 2009, 1791: 584-593 |
[74] | Natuo Koˆmoto, Guo–Xing Quan, Hideki Sezutsu, et al. A single–base deletion in an ABC transporter gene causes White eyes, White eggs,and translucent larval skin in the silkworm w–3oe mutant. Insect Biochemistry and Molecular Biology 2009, 39: 152–156. |
[75] | Kuwana H, Shimizu-Nishikawa K, Iwahana H, et al. Molecular cloning and characterization of the ABC transporter expressed in Trachea (ATET) gene from Drosophila melanogaster. Biochim Biophys Acta 1996, 1309: 47-52. |
[76] | Campbell JL, Nash HA. Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster. Neurobiol 2001, 49: 339-349. |
[77] | Lee HG, Kim YC, Dunning JS, et al. Recurring ethanol exposure induces disinhibited courtship in Drosophila. PLoS ONE 2008, 3: e1391. |
APA Style
Fengpeng Li, Xuefang Wang, Ying Xu, Jinmei Wu. (2015). Characterization of ATP-binding Cassette Transporter Genes in Silkworm, Bombyx Mori. American Journal of Bioscience and Bioengineering, 3(5), 123-133. https://doi.org/10.11648/j.bio.20150305.27
ACS Style
Fengpeng Li; Xuefang Wang; Ying Xu; Jinmei Wu. Characterization of ATP-binding Cassette Transporter Genes in Silkworm, Bombyx Mori. Am. J. BioSci. Bioeng. 2015, 3(5), 123-133. doi: 10.11648/j.bio.20150305.27
AMA Style
Fengpeng Li, Xuefang Wang, Ying Xu, Jinmei Wu. Characterization of ATP-binding Cassette Transporter Genes in Silkworm, Bombyx Mori. Am J BioSci Bioeng. 2015;3(5):123-133. doi: 10.11648/j.bio.20150305.27
@article{10.11648/j.bio.20150305.27, author = {Fengpeng Li and Xuefang Wang and Ying Xu and Jinmei Wu}, title = {Characterization of ATP-binding Cassette Transporter Genes in Silkworm, Bombyx Mori}, journal = {American Journal of Bioscience and Bioengineering}, volume = {3}, number = {5}, pages = {123-133}, doi = {10.11648/j.bio.20150305.27}, url = {https://doi.org/10.11648/j.bio.20150305.27}, eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.bio.20150305.27}, abstract = {Background: ATP-binding cassette (ABC) transporters are transmembrane proteins that utilize the energy of adenosine triphosphate (ATP) binding and hydrolysis to transport various substrates across extra and intracellular membranes, including metabolic products, lipids and sterols, and drugs. They play important roles in various processes of life, especially in drug resistance, metabolism and development. Objective: Identify the ATP-binding cassette (ABC) transporter gene family and their members in the genome of silkworm, Bombyx mori. Method: Bioinformatics and phylogenetic analysis were used in the study. Results: We identified 47 ABC proteins in the silkworm genome, which possesses members of all current ABC subfamilies A to H. ABC proteins of silkworm were compared to those from worm, fruit fly and human. A high conservation of silkworm ABC transporters were observed for proteins involved in fundamental cellular processes, including the half transporters of the ABCB subfamily, which function in iron metabolism and transport of Fe/S protein precursors, and the members of subfamilies ABCD, ABCE and ABCF, which have roles in very long chain fatty acid transport. Both ABCE and F gene products may be involved in an innate immune response to viral infections. As in the fly, ABCH proteins are inverse half-transporters showing the same domain architecture as the members of the ABCG subfamily, and ABCG transporters involve in transportation of ommochrome precursors and uric acid into pigment granules and urate granules. Conclusion: These results paved the way for further study on the function of the ABC transporters in silkworm, Bombyx mori.}, year = {2015} }
TY - JOUR T1 - Characterization of ATP-binding Cassette Transporter Genes in Silkworm, Bombyx Mori AU - Fengpeng Li AU - Xuefang Wang AU - Ying Xu AU - Jinmei Wu Y1 - 2015/12/03 PY - 2015 N1 - https://doi.org/10.11648/j.bio.20150305.27 DO - 10.11648/j.bio.20150305.27 T2 - American Journal of Bioscience and Bioengineering JF - American Journal of Bioscience and Bioengineering JO - American Journal of Bioscience and Bioengineering SP - 123 EP - 133 PB - Science Publishing Group SN - 2328-5893 UR - https://doi.org/10.11648/j.bio.20150305.27 AB - Background: ATP-binding cassette (ABC) transporters are transmembrane proteins that utilize the energy of adenosine triphosphate (ATP) binding and hydrolysis to transport various substrates across extra and intracellular membranes, including metabolic products, lipids and sterols, and drugs. They play important roles in various processes of life, especially in drug resistance, metabolism and development. Objective: Identify the ATP-binding cassette (ABC) transporter gene family and their members in the genome of silkworm, Bombyx mori. Method: Bioinformatics and phylogenetic analysis were used in the study. Results: We identified 47 ABC proteins in the silkworm genome, which possesses members of all current ABC subfamilies A to H. ABC proteins of silkworm were compared to those from worm, fruit fly and human. A high conservation of silkworm ABC transporters were observed for proteins involved in fundamental cellular processes, including the half transporters of the ABCB subfamily, which function in iron metabolism and transport of Fe/S protein precursors, and the members of subfamilies ABCD, ABCE and ABCF, which have roles in very long chain fatty acid transport. Both ABCE and F gene products may be involved in an innate immune response to viral infections. As in the fly, ABCH proteins are inverse half-transporters showing the same domain architecture as the members of the ABCG subfamily, and ABCG transporters involve in transportation of ommochrome precursors and uric acid into pigment granules and urate granules. Conclusion: These results paved the way for further study on the function of the ABC transporters in silkworm, Bombyx mori. VL - 3 IS - 5 ER -