Genome-wide identification of whole ATP-binding cassette (ABC) transporters in the intertidal copepod Tigriopus japonicus

BackgroundsThe ATP-binding cassette (ABC) transporter superfamily is one of the largest transporter gene families and is observed in all animal taxa. Although a large set of transcriptomic data was recently assembled for several species of crustaceans, identification and annotation of the large ABC transporter gene family have been very challenging.ResultsIn the intertidal copepod Tigriopus japonicus, 46 putative ABC transporters were identified using in silico analysis, and their full-length cDNA sequences were characterized. Phylogenetic analysis revealed that the 46 T. japonicus ABC transporters are classified into eight subfamilies (A-H) that include all the members of all ABC subfamilies, consisting of five ABCA, five ABCB, 17 ABCC, three ABCD, one ABCE, three ABCF, seven ABCG, and five ABCH subfamilies. Of them, unique isotypic expansion of two clades of ABCC1 proteins was observed. Real-time RT-PCR-based heatmap analysis revealed that most T. japonicus ABC genes showed temporal transcriptional expression during copepod development. The overall transcriptional profile demonstrated that half of all T. japonicus ABC genes were strongly associated with at least one developmental stage. Of them, transcripts TJ-ABCH_88708 and TJ-ABCE1 were highly expressed during all developmental stages.ConclusionsThe whole set of T. japonicus ABC genes and their phylogenetic relationships will provide a better understanding of the comparative evolution of essential gene family resources in arthropods, including the crustacean copepods.

[1]  G. Paffenhöfer,et al.  Grazing and ingestion rates of nauplii, copepodids and adults of the marine planktonic copepod Calanus helgolandicus , 1971 .

[2]  J. Walker,et al.  Distantly related sequences in the alpha‐ and beta‐subunits of ATP synthase, myosin, kinases and other ATP‐requiring enzymes and a common nucleotide binding fold. , 1982, The EMBO journal.

[3]  R. Mutharasan,et al.  Disruption of ATP-binding cassette B8 in mice leads to cardiomyopathy through a decrease in mitochondrial iron export , 2012, Proceedings of the National Academy of Sciences.

[4]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[5]  Karl Kuchler,et al.  ABC proteins : from bacteria to man , 2003 .

[6]  P. A. Rea,et al.  Drosophila ABC Transporter, DmHMT-1, Confers Tolerance to Cadmium , 2009, Journal of Biological Chemistry.

[7]  André Goffeau,et al.  Complete inventory of the yeast ABC proteins , 1997, Nature Genetics.

[8]  G. Kattner,et al.  Changes in lipids during the development of Calanus finmarchicus s.l. from Copepodid I to adult , 1987 .

[9]  J. Vandekerckhove,et al.  Characterization of the ABCA transporter subfamily: identification of prokaryotic and eukaryotic members, phylogeny and topology. , 2003, Journal of molecular biology.

[10]  André W. Visser,et al.  Lipids, buoyancy and the seasonal vertical migration of Calanus finmarchicus , 1999 .

[11]  Christian Kandt,et al.  ATP-binding cassette transporters in Escherichia coli. , 2008, Biochimica et biophysica acta.

[12]  Identification of the Anopheles gambiae ATP-binding cassette transporter superfamily genes. , 2003, Molecules and cells.

[13]  M. O'Donnell,et al.  Transepithelial transport of fluorescent p-glycoprotein and MRP2 substrates by insect Malpighian tubules: confocal microscopic analysis of secreted fluid droplets , 2005, Journal of Experimental Biology.

[14]  D. Garza,et al.  The E23 early gene of Drosophila encodes an ecdysone-inducible ATP-binding cassette transporter capable of repressing ecdysone-mediated gene activation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  T. Rouault.  Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease , 2012, Disease Models & Mechanisms.

[16]  Rosalinde Masereeuw,et al.  Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. , 2008, Trends in pharmacological sciences.

[17]  S. Almashanu,et al.  Peroxisomal ABC transporters. , 1998, Methods in enzymology.

[18]  E. Tarling.  Expanding roles of ABCG1 and sterol transport , 2013, Current opinion in lipidology.

[19]  P. A. Rea,et al.  Plant ABC proteins--a unified nomenclature and updated inventory. , 2008, Trends in plant science.

[20]  Michael Dean,et al.  Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. , 2005, Annual review of genomics and human genetics.

[21]  K. Ligon,et al.  p16INK4a induces an age-dependent decline in islet regenerative potential , 2006, Nature.

[22]  M. Welsh,et al.  Structure and function of the CFTR chloride channel. , 1999, Physiological reviews.

[23]  Jehee Lee,et al.  Cloning and expression of ecdysone receptor (EcR) from the intertidal copepod, Tigriopus japonicus. , 2010, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[24]  L. Tian,et al.  Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori , 2011, BMC Genomics.

[25]  T. Ikeda,et al.  Effect of temperature on development, growth and reproduction in the marine copepod Pseudocalanus newmani at satiating food condition , 2003 .

[26]  Richard M. Clark,et al.  A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae , 2013, BMC Genomics.

[27]  S. Leevers,et al.  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* , 2007, Journal of Biological Chemistry.

[28]  G. Cox,et al.  Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. , 1999, Biochimica et biophysica acta.

[29]  Paul T. Tarr,et al.  ATP-binding cassette transporter G1 and lipid homeostasis , 2006, Current opinion in lipidology.

[30]  Zhanjiang Liu,et al.  Genome-Wide Identification, Characterization and Phylogenetic Analysis of 50 Catfish ATP-Binding Cassette (ABC) Transporter Genes , 2013, PloS one.

[31]  N. Perrimon,et al.  Inactivation of Drosophila Huntingtin affects long-term adult functioning and the pathogenesis of a Huntington’s disease model , 2009, Disease Models & Mechanisms.

[32]  T. Roepke,et al.  Increase in multidrug transport activity is associated with oocyte maturation in sea stars * , 2006, Development, growth & differentiation.

[33]  S. Falk‐Petersen,et al.  The lipid biochemistry of calanoid copepods , 1988, Hydrobiologia.

[34]  D. Baillie,et al.  The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes , 2004, Genome Biology.

[35]  F. Kibenge,et al.  Evidence for changes in the transcription levels of two putative P-glycoprotein genes in sea lice (Lepeophtheirus salmonis) in response to emamectin benzoate exposure. , 2007, Molecular and biochemical parasitology.

[36]  L. Gilbert,et al.  Control and biochemical nature of the ecdysteroidogenic pathway. , 2002, Annual review of entomology.

[37]  D. Baillie,et al.  ATP-binding cassette protein E is involved in gene transcription and translation in Caenorhabditis elegans. , 2004, Biochemical and biophysical research communications.

[38]  M. Morita,et al.  Peroxisomal ABC transporters: structure, function and role in disease. , 2012, Biochimica et Biophysica Acta.

[39]  M. Lorenzen,et al.  Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum , 2013, BMC Genomics.

[40]  B. Hansen,et al.  Food size spectra, ingestion and growth of the copepodAcartia tonsa during development: Implications for determination of copepod production , 1988 .

[41]  J. Bresciani.  The fine structure of the integument of free-living and parasitic copepods. A review , 1986 .

[42]  T. Van Leeuwen,et al.  The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. , 2014, Insect biochemistry and molecular biology.

[43]  Michael Dean,et al.  The ABC transporter gene family of Daphnia pulex , 2009, BMC Genomics.

[44]  A. Goffeau,et al.  Fungal PDR transporters: Phylogeny, topology, motifs and function. , 2010, Fungal genetics and biology : FG & B.

[45]  S. Stefanov,et al.  Evolution of the vertebrate ABC gene family: analysis of gene birth and death. , 2006, Genomics.

[46]  O. Shirihai,et al.  Mitochondrial ABC transporters function: the role of ABCB10 (ABC-me) as a novel player in cellular handling of reactive oxygen species. , 2012, Biochimica et biophysica acta.

[47]  Xu Han,et al.  The biological regulation of ABCE1 , 2012, IUBMB life.

[48]  R. Dérand,et al.  SUR, ABC proteins targeted by KATP channel openers. , 2005, Journal of molecular and cellular cardiology.

[49]  K. Leung,et al.  The copepod Tigriopus: a promising marine model organism for ecotoxicology and environmental genomics. , 2007, Aquatic toxicology.

[50]  Jue Chen,et al.  Structure, Function, and Evolution of Bacterial ATP-Binding Cassette Systems , 2008, Microbiology and Molecular Biology Reviews.

[51]  A. Rzhetsky,et al.  The human ATP-binding cassette (ABC) transporter superfamily. , 2001, Genome research.

[52]  T. Roepke,et al.  Activation of multidrug efflux transporter activity at fertilization in sea urchin embryos (Strongylocentrotus purpuratus). , 2004, Developmental biology.

[53]  T. Snell,et al.  Estrogenic compounds affect development of harpacticoid copepod Tigriopus japonicus , 2003, Environmental toxicology and chemistry.

[54]  A. Ilias,et al.  The dMRP/CG6214 gene of Drosophila is evolutionarily and functionally related to the human multidrug resistance‐associated protein family , 2004, Insect molecular biology.

[55]  D. T. Sullivan,et al.  Subcellular localization of the first three enzymes of the ommochrome synthetic pathway in Drosophila melanogaster. , 1974, The Journal of experimental zoology.

[56]  A novel ABC transporter: the first insight into zebrafish (Danio rerio) ABCH1. , 2010, Marine environmental research.

[57]  Robert H. Silverman,et al.  Expression cloning of 2-5A-dependent RNAase: A uniquely regulated mediator of interferon action , 1993, Cell.

[58]  Jacques Meyer,et al.  Iron–sulfur protein folds, iron–sulfur chemistry, and evolution , 2008, JBIC Journal of Biological Inorganic Chemistry.

[59]  W. Kaminski,et al.  ABC A-subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport. , 2007, Frontiers in bioscience : a journal and virtual library.

[60]  Daxi Sun,et al.  Identification of a mammalian mitochondrial porphyrin transporter , 2006, Nature.

[61]  D. Epel,et al.  ABCB- and ABCC-type transporters confer multixenobiotic resistance and form an environment-tissue barrier in bivalve gills. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[62]  D. Yamamoto,et al.  Molecular cloning and characterization of the ABC transporter expressed in Trachea (ATET) gene from Drosophila melanogaster. , 1996, Biochimica et biophysica acta.

[63]  G. LeBlanc.  Crustacean endocrine toxicology: a review , 2007, Ecotoxicology.

[64]  I. Kerr.  Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. , 2004, Biochemical and biophysical research communications.

[65]  Molecular and Functional Analysis of Three Fatty Acyl-CoA Reductases with Distinct Substrate Specificities in Copepod Calanus finmarchicus , 2012, Marine Biotechnology.

[66]  D. Yamamoto,et al.  Molecular cloning and characterization of the ABC transporter expressed in Trachea (ATET) gene fromDrosophila melanogaster , 1996 .

[67]  J. Rhee,et al.  The copepod Tigriopus japonicus genomic DNA information (574Mb) and molecular anatomy. , 2010, Marine environmental research.

[68]  A. Driessen,et al.  Phylogenetic analysis of fungal ABC transporters , 2010, BMC Genomics.

[69]  C. Proud,et al.  ABC50 Interacts with Eukaryotic Initiation Factor 2 and Associates with the Ribosome in an ATP-dependent Manner* , 2000, The Journal of Biological Chemistry.

[70]  H. Andersen,et al.  Development of copepod nauplii to copepodites—a parameter for chronic toxicity including endocrine disruption , 2001, Environmental toxicology and chemistry.

[71]  T. Janvilisri,et al.  ATP-binding cassette multidrug transporters in Indian-rock oyster Saccostrea forskali and their role in the export of an environmental organic pollutant tributyltin. , 2007, Aquatic toxicology.

[72]  J. Kutok,et al.  The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulfur cluster biogenesis. , 2006, Human molecular genetics.

[73]  R. Tampé,et al.  Structural Organization of Essential Iron-Sulfur Clusters in the Evolutionarily Highly Conserved ATP-binding Cassette Protein ABCE1* , 2007, Journal of Biological Chemistry.

[74]  H. 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-3(oe) mutant. , 2009, Insect biochemistry and molecular biology.