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Insulin-like growth factor I of Japanese eel, Anguilla japonica: cDNA cloning, tissue distribution, and expression after treatment with growth hormone and seawater acclimation

Fish Physiology and Biochemistry volume 32, pages 189–201 (2006)Cite this article

Abstract

In an attempt to understand growth regulation in the Japanese eel, Anguilla japonica, we cloned insulin-like growth factor-I (IGF-I) cDNAs and examined their mRNA expression in several tissues. Two eel IGF-I (eIGF-I) cDNAs encoding preprohormones, eIGF-I-Ea1and eIGF-I-Ea2, were cloned from the liver by polymerase chain reaction (PCR). The preproIGF-Is were identical in signal peptide and mature IGF-I, but different in the E domain—eIGF-I-Ea2 mRNA was 36 bp longer than eIGF-I-Ea1 mRNA. Eel IGF-I was 83–94% identical with that of teleosts, 71% identical with that of dogfish, 87% identical with that of bullfrog and chicken, and 83% identical with that of humans. In both males and females the highest eIGF-I-Ea1 mRNA levels were observed in the liver, with detectable levels also found in the gills, heart, stomach, spleen, kidney, intestine, swim-bladder, muscle, and gonads. eIGF-I-Ea1 mRNA levels in the liver were higher in females than in males whereas in the intestine they were lower than in males. eIGF-I-Ea2 mRNA was detected in all the tissues examined and at similar levels in males and females. In this experiment higher eIGF-I-Ea1 mRNA levels were observed in the liver of larger glass eels than in those of smaller fish. eIGF-I-Ea2 mRNA levels were also higher in larger eels, although they were lower than IGF-I-Ea1 mRNA levels. Both eIGF-I mRNA levels in liver were positively correlated with the body size of the␣glass eels. Intraperitoneal injection of recombinant eel GH (reGH), 0.25 µg g−1 body weight, into glass eels resulted in a significant increase in both eIGF-I mRNAs in the liver 1 day after injection compared with control fish, but no elevation was observed 2 days after injection. Incubation of liver slices with reGH at concentrations of 10, 100, and 1,000 ng  mL−1 for 24 h resulted in a significant concentration-dependent increase in the levels of both eIGF-I mRNAs. Higher levels of eIGF-I-Ea1 and Ea2 mRNA were observed in the gills ofseawater-reared eels than in those of freshwater-reared fish, but no differenceswere observed in the whole kidney. These results suggest that IGF-I is involved in the regulation of somatic growth and also in adaptation of the Japanese eel to seawater.

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Abbreviations

GH:

Growth hormone

IGF-I:

Insulin-like growth factor-I

PCR:

Polymerase chain reaction

References

  • Ayson FG, de Jesus EGT, Moriyama S, Hyodo S, Funkenstein B, Gertler A, Kawauchi H (2002) Differential expression of insulin-like growth factor I and II mRNAs during embryogenesis and early larval development in rabbitfish, Siganus guttatus. Gen Comp Endocrinol 126:165–174

    Article  PubMed  CAS  Google Scholar 

  • Beckman BR, Dickhoff WW (1998) Plasticity of smolting chinook salmon: relation to growth and insulin-like growth factor-I. J Fish Biol 52:808–826

    Article  Google Scholar 

  • Biga PR, Schelling GT, Hardy RW, Cain KD, Overturf K, Ott TL (2004) The effects of recombinant bovine somatotropin (rbST) on tissue IGF-I, IGF-I receptor, and GH mRNA levels in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 135:324–333

    Article  PubMed  CAS  Google Scholar 

  • Caelers A, Berishvili G, Meli ML, Eppler E, Reinecke M (2004) Establishment of a real-time RT-PCR for the determination of absolute amounts of IGF-I and IGF-II gene expression in liver and extrahepatic sites of the tilapia. Gen Comp Endocrinol 137:196–204

    Article  PubMed  CAS  Google Scholar 

  • Cao Q-P, Duguay SJ, Plisetskaya EM, Steiner DF, Chan SJ (1989) Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA. Mol Endocrinol 3:2005–2010

    PubMed  CAS  Google Scholar 

  • Chen MH, Lin G, Gong H, Weng C, Chang C, Wu J (2001) The characterization of prepro-insulin-like growth factor-1 Ea-2 expression and insulin-like growth factor-1 genes (devoid 81 bp) in the zebrafish (Danio rerio). Gene 268:67–75

    Article  PubMed  CAS  Google Scholar 

  • Chen TT, Shamblott M, Lin CM, Tang Y-L, Chan K-M, Cheng CM, Yang B-Y, Marsh A (1994) Structure and evolution of fish growth hormone and insulin-like growth factor genes. In: Davey KG, Tobo SS, Peter DE (eds) Perspective in comparative endocrinology. National Research Council of Canada, Toronto, Canada, pp 352–364

    Google Scholar 

  • Chiba H, Iwatsuki K, Hayami K, Yamauchi K (1993) Effects of dietary estradiol-17β on feminization, growth and body composition in the Japanese eel (Anguilla japonica). Comp Biochem Physiol 106A:367–371

    CAS  Google Scholar 

  • de Jesus EGT, Ayson FG, Amemiya Y, Moriyama S, Hyodo S, Hirano T, Kawauchi H (2002) Milkfish (Chanos chanos) growth hormone cDNA cloning and mRNA expression in embryos and early larval stages. Aquaculture 208:177–181

    Article  Google Scholar 

  • Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S

    PubMed  CAS  Google Scholar 

  • Duan C, Duguay SJ, Plisetskaya EM (1993) Insulin-like growth factor I (IGF-I) mRNA expression in coho salmon, Oncorhynchus kisutch: tissue distribution and effects of growth hormone/prolactin family proteins. Fish Physiol Biochem 11:371–379

    Article  CAS  Google Scholar 

  • Duan C, Hirano T (1992) Effects of insulin-like growth factor-I and insulin on the in-vitro uptake of sulphate by eel branchial cartilage: evidence for the presence of independent hepatic and pancreatic sulphation factors. J Endocrinol 133:211–219

    PubMed  CAS  Google Scholar 

  • Duan C, Inui Y (1990) Evidence for the presence of a somatomedin-like plasma factor(s) in the Japanese eel, Anguilla japonica. Gen Comp Endocrinol 79:326–331

    Article  PubMed  CAS  Google Scholar 

  • Duan C, Plisetskaya EM, Dickhoff WW (1995) Expression of insulin-like growth factor I in normally and abnormally developing coho salmon (Oncorhynchus kisutch). Endocrinology 136:446–452

    Article  PubMed  CAS  Google Scholar 

  • Duguay SJ, Chan SJ, Mommsen TP, Steiner DF (1995) Divergence of insulin-like growth factors I and II in the elasmobranch, Squalus acanthias. FEBS Lett 371:69–72

    Article  PubMed  CAS  Google Scholar 

  • Duguay SJ, Lai-Zhang J, Steiner DF, Funkenstein B, Chan SJ (1996) Developmental and tissue-regulated expression of IGF-I and IGF-II mRNAs in Sparus aurata. J Mol Endocrinol 16:123–132

    PubMed  CAS  Google Scholar 

  • Duguay SJ, Park LK, Samadpour M, Dickhoff WW (1992) Nucleotide sequence and tissue distribution of three insulin-like growth factor I prohormone in salmon. Mol Endocrinol 6:1202–1210

    Article  PubMed  CAS  Google Scholar 

  • Duguay SJ, Swanson P, Dickhoff WW (1994) Differential expression and hormonal regulation of alternatively spliced IGF-I mRNA transcripts in salmon. J Mol Endocrinol 12:25–37

    PubMed  CAS  Google Scholar 

  • Inoue K, Iwatani H, Takei Y (2003) Growth hormone and insulin-like growth factor-I of a euryhaline fish Cottus kazika: cDNA cloning and expression after seawater acclimation. Gen Comp Endocrinol 131:77–84

    Article  PubMed  CAS  Google Scholar 

  • Kajimoto Y, Rotwein P (1989) Structure and expression of a chicken insulin-like growth factor I precursor. Mol Endocrinol 3:1907–1913

    Article  PubMed  CAS  Google Scholar 

  • Kajimoto Y, Rotwein P (1990) Evolution of insulin-like growth factor I (IGF-I): structure and expression of an IGF-I precursor from Xenopus laevis. Mol Endocrinol 4:217–225

    PubMed  CAS  Google Scholar 

  • Kawauchi H, Suzuki K, Yamazaki T, Moriyama S, Nozaki M, Yamaguchi K, Takahashi A, Youson J, Sower SA (2002) Identification of growth hormone in the sea lamprey, an extant representative of a group of the most ancient vertebrates. Endocrinology 143:4916–4921

    Article  PubMed  CAS  Google Scholar 

  • Kermouni A, Mahmoud SS, Wang S, Moloney M, Habibi HR (1998) Cloning of a full-length insulin-like growth factor-I complementary DNA in the goldfish liver and ovary and development of a quantitative PCR method for its measurement. Gen Comp Endocrinol 111:51–60

    Article  PubMed  CAS  Google Scholar 

  • Kishida M, Hirano T (1988) Development of radioimmunoassay for eel growth hormone. Nippon Suisan Gakkaishi 54:1321–1327

    CAS  Google Scholar 

  • Kishida M, Hirano T, Kubokawa J, Hasegawa S, Kawauchi H, Yamaguchi K, Shirahata K (1987) Isolation of two forms of growth hormone secreted from eel pituitaries in vitro. Gen Comp Endocrinol 65:478–488

    Article  PubMed  CAS  Google Scholar 

  • Liang YH, Cheng CH, Chan KM (1996) Insulin-like growth factor IEa2 is the predominantly expressed form of IGF in common carp (Cyprinus carpio). Mol Mar Biol Biotechnol 5:145–152

    PubMed  CAS  Google Scholar 

  • Loffing-Cueni D, Schmid AC, Graf H, Reinecke M (1998) IGF-I in the bony fish Cottus scorpius: cDNA, expression and differential localization in brain and islets. Mol Cell Endocrinol 141:187–194

    Article  PubMed  CAS  Google Scholar 

  • Mancera JM, McCormick SD (1998) Osmoregulatory actions of the GH/IGF axis in non-salmonid teleosts. Comp Biochem Physiol 121B:43–48

    CAS  Google Scholar 

  • Marchekidom J, Schmitz M, Houdebine LM, Vidal B, Le Belle N, Dufour S (1996) Development of a radioimmunoassay for European eel growth hormone and application to the study of silvering and experimental fasting. Gen Comp Endocrinol 102:360–369

    Article  Google Scholar 

  • Matsui I (1952) Studies on the morphology, ecology and pondculture of the Japanese eel (Anguilla japonica, Temminck and Schlegel). J Shimonoseki Fish Col 2:1–245

    Google Scholar 

  • McRory JE, Sherwood NM (1994) Catfish express two forms of insulin-like growth factor-I (IGF-I) in the brain. Ubiquitous IGF-I and brain-specific IGF-I. J Biol Chem 269:18588–18592

    PubMed  CAS  Google Scholar 

  • Moriyama S, Shimma H, Tagawa T, Kagawa H (1997) Changes in plasma insulin-like growth factor-I levels in precociously maturing amago salmon, Oncorhynchus masou ishikawai. Fish Physiol Biochem 17:253–259

    Article  CAS  Google Scholar 

  • Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotechnol Biochem 64:1553–1562

    Article  PubMed  CAS  Google Scholar 

  • Nagamatsu S, Chan SJ, Falkmer S, Steiner DF (1991) Evolution of the insulin gene superfamily. Sequence of a preproinsulin-like growth factor cDNA from the Atlantic hagfish. J Biol Chem 266:2397–2402

    PubMed  CAS  Google Scholar 

  • Pierce AL, Beckman BR, Shearer KD, Larsen DA, Dickhoff WW (2001) Effects of ration on somatotropic hormones and growth in coho salmon. Comp Biochem Physiol 128B:255–264

    CAS  Google Scholar 

  • Reinecke M, Bjoronsson BT, Dickhoff WW, McCormick SD, Navorro I, Power DM, Gutierrez J (2005) Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142:20–24

    Article  PubMed  CAS  Google Scholar 

  • Reinecke M, Collet C (1998) The phylogeny of the insulin-like growth factors. Int Rev Cytol 183:1–94

    Article  PubMed  CAS  Google Scholar 

  • Reinecke M, Schmid A, Ermatinger R, Loffing-Cueni D (1997) Insulin-like growth factor I in the teleost Oreochromis mossambicus, the tilapia: gene sequence, tissue expression, and cellular localization. Endocrinology 138:3613–3619

    Article  PubMed  CAS  Google Scholar 

  • Rotwein P, Pollock KM, Didier DK, Krivi GG (1986) Organization and sequence of human insulin-like growth factor I gene. J Biol Chem 261:4828–4832

    PubMed  CAS  Google Scholar 

  • Sakamoto T, Hirano T (1993) Expression of insulin-like growth factor I gene in osmoregulatory organs during seawater adaptation of the salmonid fish: possible mode of osmoregulatory action of growth hormone. Proc Natl Acad Sci USA 90:1912–1916

    Article  PubMed  CAS  Google Scholar 

  • Stahlbom AK, Sara VR, Hoeben P (1999) Insulin-like growth factor mRNA in Barramundi (Lates calcarifer): alternative splicing and nonresponsiveness to growth hormone. Biochem Genetics 37:69–93

    Article  CAS  Google Scholar 

  • Tanaka M, Taniguchi T, Yamamoto I, Sakaguchi K, Yosizato H, Ohkubo T, Nakashima K (1998) Gene and cDNA structure of flounder insulin-like growth factor-I (IGF-I): multiple mRNA species encode a single short mature IGF-I. DNA Cell Biol 17:859–868

    Article  PubMed  CAS  Google Scholar 

  • Tian XC, Chen MJ, Pantschenko AG, Yang TJ, Chen TT (1999) Recombinant E-peptides of pro-IGF-I have mitogenic activity. Endocrinology 140:3387–3390

    Article  PubMed  CAS  Google Scholar 

  • Vong QP, Chan KM, Cheng CH (2003) Quantification of common carp (Cyprinus carpio) IGF-I and IGF-II mRNA by real-time PCR: differential regulation of expression by GH. J Endocrinol 178:513–521

    Article  PubMed  CAS  Google Scholar 

  • Wallis AE, Devlin RH (1993) Duplicate insulin-like growth factor-I genes in salmon display alternative splicing pathways. Mol Endocrinol 7:409–422

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported in part by a Grant-in aid for Encouragement of Young Scientists (12760131) from the Ministry of Education, Science and Culture to S.M. and also from the Fisheries Agency to H.K. and S.M.

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Authors and Affiliations

  1. School of Fisheries Sciences, Kitasato University, Sanriku, Iwate, 022-0101, Japan

    Shunsuke Moriyama, Kiyoko Yamaguchi, Tomomi Takasawa, Hiroaki Chiba & Hiroshi Kawauchi

  2. Medical-Technology, Kitasato Junior College of Health and Hygienic Sciences, Yamato, Niigata, 949-7241, Japan

    Kiyoko Yamaguchi

Authors
  1. Shunsuke Moriyama
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  2. Kiyoko Yamaguchi
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  3. Tomomi Takasawa
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  4. Hiroaki Chiba
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  5. Hiroshi Kawauchi
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Correspondence to Shunsuke Moriyama.

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Moriyama, S., Yamaguchi, K., Takasawa, T. et al. Insulin-like growth factor I of Japanese eel, Anguilla japonica: cDNA cloning, tissue distribution, and expression after treatment with growth hormone and seawater acclimation. Fish Physiol Biochem 32, 189–201 (2006). https://doi.org/10.1007/s10695-006-0011-8

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  • DOI: https://doi.org/10.1007/s10695-006-0011-8

Keywords

  • Cloning
  • Growth
  • Growth hormone
  • Insulin-like growth factor-I
  • Japanese eel
  • mRNA expression

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