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Expression of Pancreatic Enzyme Genes During the Early Larval Stage of Japanese Eel Anguilla Japonica

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Expression of Pancreatic Enzyme Genes During the Early Larval Stage of Japanese Eel Anguilla Japonica FISHERIES SCIENCE 2002; 68: 736–744 Expression of pancreatic enzyme genes during the early larval stage of Japanese eel Anguilla japonica Tadahide KUROKAWA,* Tohru SUZUKI, Hiromi OHTA, Hirohiko KAGAWA, Hideki TANAKA AND Tatsuya UNUMA National Research Institute of Aquaculture, Fisheries Research Agency, Nansei, Mie 516-0193, Japan ABSTRACT: To reveal the ontogeny of pancreatic exocrine function in the early larval stage of eel, cDNAs encoding major pancreatic enzymes, trypsinogen, amylase and lipase were identified from the Japanese eel Anguilla japonica and their expression pattern in larvae was analyzed. The cloned eel trypsinogen precursor consisted of 224 amino acids and showed 82.2% identity to trypsinogen- 2 of winter flounder Pleuronectes americanus. The eel amylase precursor consisted of 512 amino acids and showed 77% identity to winter flounder amylase. Eel pancreatic lipase was composed of 470 amino acids and had 58.3% of identity to human pancreatic lipase. In the eel larvae, mRNA expression of trypsinogen and amylase was first detected at 6 days post-hatching (d.p.h.), and the expression level increased between 7 and 8 d.p.h. In contrast, mRNA expression of lipase was first detected at 8 d.p.h. Eel larvae start to feed actively at 8 d.p.h. Thus, it was indicated that eel pan- creas starts to synthesize digestive enzymes at 6 d.p.h. and acquires full function by the onset of exogenous feeding at 8 d.p.h. KEY WORDS: amylase, cDNA, eel, larvae, lipase, mRNA expression, pancreatic enzymes, trypsinogen. INTRODUCTION digestive tract of wild Anguilliformes leptocephali feces of zooplankton and larvacean house were Anguilliformes, including eel, have a unique larval found.8 However, the natural food of eel prelepto- stage called leptocephalus.1 Tsukamoto2 estimated cephali is still unknown. Therefore, studies of the that the spawning area of the Japanese eel Anguilla digestive physiology in the larval stage are very japonica was west of the Mariana Islands where important for the development of a suitable diet many young leptocephali were collected. However, and culture systems for eel larvae. wild preleptocephali and eggs of Japanese eel have The pancreas is a very important organ for not yet been found. digestion, particularly in the larval stage in which Under experimental conditions, Yamamoto and the stomach is not yet developed.9 In most teleosts, Yamauchi3 first succeeded in producing Japanese it is difficult to collect pure pancreas because the eel larvae (preleptocephalus). In spite of many pancreatic tissue is diffusively distributed.10,11 Eel researchers’ efforts, there has been only one suc- is one of the few teleosts possessing a compact cessful report on growing larvae to the lepto- exocrine pancreas; therefore, the eel is adequate cephalus stage.4 Fertilized eggs and hatched larvae for the biochemical characterization of the pan- have also been obtained in the European eel creatic enzymes.12,13 However, when analyzing the Anguilla anguilla5,6 and the New Zealand eel synthetic ability of digestive enzymes in larvae, Anguilla dieffenbachii,7 but rearing larvae was gene expression analysis is more specific than unsuccessful. biochemical detection because some enzymes, A lack of information about the diet of larvae is which have the same activity as pancreatic probably one of the major reasons for their short enzymes, exist in other organs. In the present survival period in experimental conditions. In the study, we cloned cDNAs encoding the major pancreatic enzymes, trypsinogen, amylase and lipase, from the Japanese eel and analyzed their *Corresponding author: Tel: 81-599-66-1830. Fax: 81-599-66- expression patterns during the larval stage in order 1962. Email: [email protected] to reveal the development of enzyme synthetic Received 7 September 2001. Accepted 17 December 2001. ability in the eel larval pancreas. Pancreatic enzyme genes of eel FISHERIES SCIENCE 737 MATERIALS AND METHODS PCR products of the expected length for trypsino- gen (530 bp), amylase (650 bp) and lipase (540 bp) Polymerase chain reaction amplification were purified from agarose gel and cloned into the pCRII vector (Invitrogen, Carlsbad, CA, USA). The pancreas (0.1 g) of Japanese eel Anguilla Inserts were sequenced using the Big Dye Termi- japonica (38 cm in total length, 2-year-old male) nator Cycle Sequencing FS Ready Reaction Kit was dissected and poly (A) + RNA was prepared (Applied Biosystems, Foster City, CA, USA) and using the QuickPrep mRNA Purification Kit an automated DNA sequencer (377 A; Applied (Amersham Pharmacia Biotech, Piscataway, NJ, Biosystems). USA). First-strand cDNA linked with 5¢- and 3¢- adapters for rapid amplification for cDNA ends (RACE) was synthesized using the SMART PCR cDNA amplification by 5¢- and 3¢-rapid cDNA Library Construction Kit (Clontech, Palo amplification for cDNA ends Alto, CA, USA). The primary polymerase chain reaction (PCR) Rapid amplification for cDNA ends PCRs (5¢- and primers (Table 1) were designed at the conserved 3¢-) were performed using primers designed in region of vertebrate trypsinogen (winter flounder, the adapter sequences of the SMART PCR cDNA GenBank AAC32752; Japanese flounder, BAA82362; Library Construction Kit and first and second sea bass, CAA07315), amylase (winter flounder, gene-specific primers designed in the cloned PCR AF252633; mouse, P00688) and pancreatic lipase fragments (Table 2), as previously described.14 The (mouse, A34671; human, C43357; rabbit, A28997). PCR parameters were 30 cycles of 95°C for 30 s, The cDNA of pancreas was used as a template for 58°C for 1 min, and 72°C for 2 min both for first and the primary PCR. Polymerase chain reactions were second PCRs. The RACE PCR products were puri- performed using primer sets, Try5¢ and 3¢ for fied from the gel, cloned into the pCRII vector and trypsinogen, Amy5¢ and 3¢ for amylase and Lip5¢ sequenced. and 3¢ for lipase, with Taq polymerase and an additional buffer (Takara, Ohtsu, Japan). The PCR parameters for trypsinogen were 30 cycles of 96°C Reverse transcription-PCR assay in larvae for 30 s, 50°C for 1 min, and 72°C for 2 min The parameters for amylase and lipase were 50 cycles Fertilized eggs of the Japanese eel were kept in a of 96°C for 30 s, 42°C for 1 min and 72°C for 2 min. 50 L tank supplied with running seawater (21 ± 1°C) Table 1 Primer sequences of primary polymerase chain reaction for trypsinogen (Try), amylase (Amy) and lipase (Lip) 5¢ Primer 3¢ Primer Try5¢-CAYCAGGTGTCTCTGAAC Try3¢-CCCARGACACAACACCCTG Amy5¢-GCNTGYAARCAYATGTGGCC Amy3¢-SWYTGRTTRTCCCACCAGTT Lip5¢-AAYTGYATHTGYGTNGAYTGG Lip3¢-AWRTCNGCRTAYTTRTA Table 2 Primer sequences of rapid amplification for cDNA ends–polymerase chain reaction 5¢RACE 3¢RACE RACE adapter primer RACE5¢a-GCAGTGGTATCAACGCAGAGTGGCCA RACE3¢a-TAGAGGCCGAGGCGGCCGACAT RACE5¢b-GGTATCAACGCAGAGTGGCCATTACG RACE3¢b-AGGCCGAGGCGGCCGACATGTT Gene-specific primer Try5¢a-GAGTTTGAACAGTCGCTCTCC Try3¢a-TTCATCGGCGCTTCCCACGTC Try5¢b-ACCCAGGCGCACTTCCAAACGGCTC Try3¢b-TGGAAATCCCCATCCTGTCGGAGAG Amy5¢a-GGGCCAGCATAAAACCTGTGG Amy3¢a-TACTGGAATTGGTCGGGTCAC Amy5¢b-GCTGGACACAGCCTGCAGGTC Amy3¢b-GGTCATTTTCCGTAATGTTGTC Lip5¢a-AAGATGGCCGACAGCTTGAGC Lip3¢a-CCAGCAGAGGCCCGAGTCGGT Lip5¢b-GTACAGCGTCCGGCCGCCCTT Lip3¢b-GGCCTGCAACCATCTGAGGTC 738 FISHERIES SCIENCE T Kurokawa et al. circulating at a flow rate of 1.2 L/min. Larvae RESULTS hatched 2 days post fertilization. From 7 days post- hatching (d.p.h.), larvae were kept in 5 L acrylic Cloning of eel pancreatic enzyme cDNA resin bowl tanks and reared by the culture system developed by Tanaka et al.4 using Aquaran (BASF, Sequence analysis indicated that trypsinogen Tokyo, Japan) as the diet. (544 bp), amylase (653 bp) and lipase (518 bp) Messenger RNA of whole larvae was prepared cDNA fragments were amplified from the eel pan- at 0, 1, 3, 4, 6, 7, 8, 9 and 10 d.p.h. (five individuals creas by PCR using degenerated primers (Table 1). were pooled at each stage) using the QuickPrep The full sequences of eel trypsiogen, amylase and mRNA Purification Kit (Amersham Pharmacia lipase cDNA were successfully obtained by 5¢- and Biotech) and cDNA was synthesized using First- 3¢-RACE amplifications using primers designed strand cDNA Synthesis Kit (Amersham Pharmacia from the sequences of the cloned PCR fragments. Biotech). The eel trypsinogen precursor (GenBank Polymerase chain reaction was performed using AB070720) that was obtained consisted of 244 primer sets for RT-PCR (Table 3). The PCR para- amino acids including a putative 15-amino-acid meters were 30 cycles of 95°C for 30 s, 60°C for signal peptide and five-amino-acid activation 1 min and 72°C for 2 min Eel b-actin was amplified peptide (Fig. 1). The eel trypsinogen has a high to confirm the steady-state level of expression of identity to winter flounder trypsinogen-2 (82.2%), the housekeeping gene. Japanese flounder trypsinogen-1 (78.1%) and Maori cod (76.9%). The eel amylase precursor (GenBank AB070721) In situ hybridization consisted of 512 amino acids. The position of the cleavage site for a signal peptide was conserved Antisense riboprobes were transcribed from after position 15 alanine, as in the case of winter the clones of primary PCR amplification for flounder and mouse amylase (Fig. 2). The eel trypsin, amylase and lipase using the Boehringer amylase showed a high identity to the amylase of Mannheim RNA Labeling Kit (Boehringer winter flounder (77%) and mouse (72.6%). Mannheim, Basel, Switzerland) with digoxigenin The eel lipase precursor (GenBank AB070722) (DIG)-UTP. Sense riboprobes were also tran- consisted of 470 amino acids
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