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Isolation of Novel Hepcidin Isoforms from the Rockbream Oplegnathus Fasciatus (Perciformes)

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Isolation of Novel Hepcidin Isoforms from the Rockbream Oplegnathus Fasciatus (Perciformes) Fish Aqua Sci 14(1), 31-42, 2011 31 Isolation of Novel Hepcidin Isoforms from the Rockbream Oplegnathus fasciatus (Perciformes) Sang Yoon Lee and Yoon Kwon Nam* Department of Marine Bio-Materials and Aquaculture, Pukyong National University, Busan 608-737, Korea Three novel hepcidin isoforms were isolated and characterized from the perciform fish species Oplegnathus fasciatus. These hepcidin isoforms (designated rbhepc5, rbhepc6 and rbhepc7) were found to share a conserved, tripartite gene structure and a considerable sequence homology one another. A comparison of their mature peptide sequences with those of other perciform hepcidin orthologs indicated that these three hepcidin isoforms as well as four other isoforms previously identified in this species, appear to belong to the HAMP2 group of hepcidin genes. Analysis of the 5′-upstream sequences showed that the proximal non-coding regions of rbhepc5~7 do not possess canonical TATA signals; instead, they harbor several binding motifs for transcription factors involved in immune modulation. Reverse transcriptase-PCR analysis demonstrated that the rbhepc5~7 are expressed predominantly in the liver, and that the transcription of rbhepc5~7 is rapidly induced in the liver, but not in other tissues, by experimental challenge with any of three different bacterial species. However, transcription of rbhepc6 appeared to be negligible under both basal and stimulated conditions, as judged by the redundancy count of randomly chosen reverse transcriptase-PCR clones. Key words: Gene structure, Hepcidin isoforms, mRNA expression, Rockbream (Oplegnathus fasciatus) Introduction Darwinian selection driven by host-pathogen interaction (e.g., adaptive evolution directed by Hepcidin, also known as liver-expressed antimicro- bial peptide (LEAP), is a cysteine-rich, antimicrobial, pathogens when the host is exposed to new environ- β-sheet protein that plays a central role in the ments) has been suggested as being the force behind homeostatic regulation of iron content (Park et al., gene duplication forming the hepcidin multigene 2001; Atanasiu et al., 2006). Although mammalian family (or cluster) in the fish genome (Padhi and genomes contain only one hepcidin gene (with the Verghese, 2007; Xu et al., 2008). This hypothesis is exception of the mouse genome, which has two), supported by the results of several experimental many fish genomes possess multiple hepcidin gene studies demonstrating differential responses of isoforms; the number of hepcidin isoforms is variable hepcidin isoforms in a given species to different kinds among fish species (Shi and Camus, 2006). Species of infectious agents (Huang et al., 2007; Cho et al., of the order Perciformes (perch-like fishes), one of 2009). Considering this evidence, it is generally the largest teleost orders, produce various hepcidin agreed that the evolutionary pathway of fish hep- transcripts that might be decoded from each separate cidins is different from one common to mammalian genomic copy (Rodrigues et al., 2006; Huang et al., hepcidins, and that isoform-specific regulation in 2007; Xu et al., 2008). The species with the highest response to environmental or physiological perturba- number of hepcidin isoforms identified thus far is the tions should be taken into account more importantly black porgy (Acanthopagrus schlegelii, order for fish hepcidins. Perciformes), which has seven unique isoforms (Yang The rockbream Oplegnathus fasciatus (order et al., 2007). Perciformes) is a commercially important and aqua- culture-relevant food fish in Korea. Although its *Corresponding author: [email protected] market demand has been gradually increasing, one of 31 32 Fish Aquat Sci 14(1), 31-42, 2011 the most significant hindrances to efficient production tions were synthesized. These primers were used for of this fish species has been frequent outbreaks of 5′-directional genome walking using a Genome- infectious diseases (Choi et al., 2006; Cho et al., Walker Universal Kit (BD Biosciences Clontech, 2009). For this reason, a better understanding of the Mountain View, CA, USA) according to the manu- immune function and defense system of this species facturer’s instructions, and 196 clones from the is needed. genome walking experiments were sequenced to A potential strategy for improving the efficiency survey for the presence of hepcidin gene copies and capacity of O. fasciatus farming is the genetic differing from rbhepc1~4 in their structural charac- manipulation of its hepcidin genes (see also Hsieh et teristics. From first-round survey primers found to be al., 2010). We recently isolated four hepcidin effective for the isolation of novel hepcidin copies, a isoforms (rbhepc1 to rbhepc4) from this species and new pair of PCR primers [rbHEPC-pDE (5′-AGGG showed that, although these isoforms vary at only a GACTGTACACCATTCACA-3′) and rbHEPC cons few amino acid (aa) residues, they are differentially RV1 (5′-ACAACTGTTGGAGCAGGAATCC-3′)] was regulated in response to different types of biological designed for the isolation of a continuous fragment stimulation (Cho et al., 2009). Because our genomic containing the novel hepcidin genes. PCR amplifica- blot hybridization analyses strongly suggested that tion was performed using the Expand High Fidelity the O. fasciatus genome harbors other hepcidin gene Plus PCR System (Roche Applied Science, Mann- copies in addition to the four identified isoforms, we heim, Germany) in a thermal cycler set for one round carried out the present study to isolate and of initial denaturation at 94°C for 3 min; 30 cycles of characterize these additional hepcidin gene copies. 94°C for 45 s, 58°C for 45 s, and 72°C for 1 min; and The ultimate aim was to gain deeper insight into the one round of final elongation at 72°C for 5 min. The interactive orchestration or diversification of the PCR products were purified using PCR Purification complete set of hepcidin isoforms in rockbream. Kit (Bioneer, Daejeon, Korea), cloned into the pGEM-T Easy Vector (Promega, Madison, WI, USA), and transformed into Escherichia coli cells. The Materials and Methods resulting clones were screened using blue/white Fish specimen and nucleic acid preparation screening with 5-bromo-4-chloro-3-indolyl-beta-D- Rockbream juveniles (body weight 80-120 g) were galactopyranoside (X-gal) and isopropyl β-D-thio- purchased from a local farm and kept in 100-L galactopyranoside (IPTG) according to the directions laboratory tanks containing water maintained at provided by Promega. Of the positive clones, 96 were 22±1°C throughout the experiment. Dissolved randomly selected for sequencing in both directions, oxygen content was 5-6 ppm. A commercial pelleted and their continuous sequences were analyzed using flounder diet (Woosung Feed Corp., Daejeon, Korea) sequence-editing software (Sequencher; Gene Codes was fed during the 1-2 week acclimation period. Corp., Ann Arbor, MI, USA). Of these sequences, Genomic DNA was prepared from whole blood or only those showing multiple hits were considered to caudal fin using the conventional SDS/proteinase K be the novel hepcidin gene copies; sequences method followed by organic extraction and ethanol showing nucleotide changes only at wobble positions precipitation (Sambrook and Russell, 2001). The (in exons) or only at a few sites in non-coding regions integrity and quantity of the prepared genomic DNA were discarded. A total of three novel hepcidin gene was confirmed by electrophoresis on ethidium copies, designated rbhepc5~7, were identified by this bromide-stained 0.3%-agarose gels and spectro- process. photometry (Gene Quant II spectrophotometer; Pharmacia Biotech, Uppsala, Sweden). Total RNA Characterization of newly identified rockbream from various tissues was purified using an RNeasy hepcidin isoform sequences Midi Kit (Qiagen, Hilden, Germany) with DNase The sequences of the newly identified hepcidin treatment, and the intact RNA was confirmed by isoforms were compared with those of other perci- determining the ratio of 28S:18S ribosomal RNA form orthologs using a BLAST search of the National (rRNA) in a 1% MOPS/formaldehyde agarose gel. Centers for Biotechnology GenBank (NCBI) database (http://ncbi.nlm.nih.gov/Blast.cgi). A multiple se- Isolation of novel hepcidin genes quence alignment of mature hepcidin peptides was Based on the sequences of other teleost hepcidin created using the ClustalW program (http://align. genes, including rbhepc1~4, various reverse primers genome.jp/). Ggene structures (exon-intron organiza- containing degenerate nucleotides at varying posi- tion) of the rockbream hepcidin isoforms were Lee and Nam Novel Hepcidin Isoforms from O. fasciatus 33 compared with those of other teleost hepcidin genes TCTAGCGGC-3′)] was included in the reverse compiled from GenBank. Additional potential fish transcription reactions to allow for normalization as hepcidin isoforms were identified by a BLAST/ Text described by Lee and Nam (2009). One microliter of search against the Ensembl genome database the resulting cDNA templates was PCR-amplified in (http://www.ensembl.org/index.html) and a tBLASTn a thermal cycler programmed for one round of initial search against the NCBI database of non-human, denaturation at 94°C for 3 min and 26 cycles (for non-mouse expressed sequence tags. Putative signal isoforms rbhepc1~4) or 35 cycles (for isoforms peptides were identified using the SignalP 3.0 Server rbhepc5~7) of 94°C for 20 s, 58°C for 20 s, and 72°C (http://www.cbs.dtu.dk/services/SignalP/), and poten- for 20 s. A 5 µL aliquot
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