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Involvement of growth hormone-insulin-like growth factor I system in cranial remodeling during halibut metamorphosis as indicated by tissue- and stage-specific receptor gene expression and the presence of growth hormone receptor protein

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Abstract

The role of growth hormone (GH) and insulin-like growth factor-I (IGF-I) in the tissue remodeling associated with the transition of a symmetrical larva to an asymmetrical juvenile during flatfish metamorphosis is unknown. In order to investigate the potential role of these hormones in the remodeling of cranial bone and soft tissue that accompanies eye migration during metamorphosis of Atlantic halibut (Hippoglossus hippoglossus) larvae, tissue-specific gene expression was monitored by in situ hybridization for Atlantic halibut type I growth hormone receptor (hhGHR), type II hhGHR, and insulin-like growth factor-I receptor (hhIGF-IR). Polyclonal antibody generated against the extracellular domain of type I hhGHR was used for the immunohistochemical localization of type I GHR protein. Type I hhGHR, type II hhGHR, and hhIGF-IR mRNA were expressed in fibroblasts, frontal bone osteocytes, and dorsal chondrocytes at the onset of metamorphosis (stage 8), during metamorphic climax (stage 9), and in fully metamorphosed juveniles (stage 10). Type I GHR protein showed similar expression patterns to those of type I hhGHR mRNA, except in chondrocytes in which little GHR protein was detected. The localization of GHR and IGF-IR transcripts and GHR protein in cranial structures that undergo remodeling is intriguing and suggests that, in addition to thyroid hormones, the GH-IGF-I system is involved in morphological transformations during metamorphosis in Atlantic halibut.

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References

  • Barnard R, Haynes KM, Werther GA, Waters MJ (1988) The ontogeny of growth hormone receptors in the rabbit tibia. Endocrinology 122:2562–2569

    PubMed  CAS  Google Scholar 

  • Berishvili G, Shved N, Eppler E, Clota F, Baroiller JF, Reinecke M (2006) Organ-specific expression of IGF-I during early development of bony fish as revealed in the tilapia, Oreochromis niloticus, by in situ hybridization and immunohistochemistry: indication for the particular importance of local IGF-I. Cell Tissue Res 325:287–301

    Article  PubMed  CAS  Google Scholar 

  • Buckbinder L, Brown DD (1993) Expression of the Xenopus laevis prolactin and thyrotropin genes during metamorphosis. Proc Natl Acad Sci USA 90:3820–3824

    Article  PubMed  CAS  Google Scholar 

  • Calduch-Giner J, Duval H, Chesnel F, Boeuf G, Perez-Sanchez J, Boujard D (2001) Fish growth hormone receptor: molecular characterization of two membrane-anchored forms. Endocrinology 142:3269–3273

    Article  PubMed  CAS  Google Scholar 

  • Calduch-Giner JA, Mingarro M, Vega-Rubin de Celis S, Boujard D, Perez-Sanchez J (2003) Molecular cloning and characterization of gilthead sea bream (Sparus aurata) growth hormone receptor (GHR). Assessment of alternative splicing. Comp Biochem Physiol [B] 136:1–13

    Article  CAS  Google Scholar 

  • Campinho MA, Silva N, Nowell MA, Llewellyn L, Sweeney G, Power D (2007a) Troponin-T isoform expression is modulated during Atlantic halibut metamorphosis. BMC Dev Biol 7:71

    Article  PubMed  CAS  Google Scholar 

  • Campinho MA, Silva N, Sweeney GE, Power DM (2007b) Molecular, cellular and histological changes in skin from a larval to an adult phenotype during bony fish metamorphosis. Cell Tissue Res 327:267–284

    Article  PubMed  CAS  Google Scholar 

  • Cheng CM, Chen TT (1995) Synergism of GH and IGF-I in stimulation of sulphate uptake by teleostean branchial cartilage in vitro. J Endocrinol 147:67–73

    PubMed  CAS  Google Scholar 

  • de Jesus EG, Hirano T, Inui Y (1993) Flounder metamorphosis: its regulation by various hormones. Fish Physiol Biochem 11:323–328

    Article  Google Scholar 

  • de Jesus EG, Hirano T, Inui Y (1994) The anti-metamorphic effect of prolactin in the Japanese flounder. Gen Comp Endocrinol 93:44–50

    Article  PubMed  Google Scholar 

  • Denver RJ, Glennemeier KA, Boorse GC (2002) Endocrinology of complex life cycles: amphibians. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, vol 2. Elsevier Science, San Diego, pp 469–513

    Google Scholar 

  • Duan C, Plisetskaya EM (1993) Nutritional regulation of insulin-like growth factor-I mRNA expression in salmon tissues. J Endocrinol 139:243–252

    Article  PubMed  CAS  Google Scholar 

  • Edens A, Talamantes F (1998) Alternative processing of growth hormone receptor transcripts. Endocr Rev 19:559–582

    Article  PubMed  CAS  Google Scholar 

  • Einarsdóttir IE, Silva N, Power DM, Smaradottir H, Björnsson BTh (2006) Thyroid and pituitary gland development from hatching through metamorphosis of a teleost flatfish, the Atlantic halibut. Anat Embryol (Berl) 211:47–60

    Article  Google Scholar 

  • Einarsdóttir IE, Anjos L, Hildahl J, Björnsson BTh, Power DM (2007) Isolation of Atlantic halibut pituitary hormones by continuous-elution electrophoresis followed by fingerprint identification, and assessment of growth hormone content during larval development. Gen Comp Endocrinol 150:355–363

    Article  PubMed  CAS  Google Scholar 

  • Eppler E, Caelers A, Shved N, Hwang G, Rahman AM, Maclean N, Zapf J, Reinecke M (2007) Insulin-like growth factor I (IGF-I) in a growth-enhanced transgenic (GH-overexpressing) bony fish, the tilapia (Oreochromis niloticus): indication for a higher impact of autocrine/paracrine than of endocrine IGF-I. Transgenic Res 16:479–489

    Article  PubMed  CAS  Google Scholar 

  • Filby AL, Tyler CR (2007) Cloning and characterization of cDNAs for hormones and/or receptors of growth hormone, insulin-like growth factor-I, thyroid hormone, and corticosteroid and the gender-, tissue-, and developmental-specific expression of their mRNA transcripts in fathead minnow (Pimephales promelas). Gen Comp Endocrinol 150:151–163

    Article  PubMed  CAS  Google Scholar 

  • Frick GP, Tai LR, Baumbach WR, Goodman HM (1998) Tissue distribution, turnover, and glycosylation of the long and short growth hormone receptor isoforms in rat tissues. Endocrinology 139:2824–2830

    Article  PubMed  CAS  Google Scholar 

  • Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Swanson P, Dickhoff WW (2005) Identification of the salmon somatolactin receptor, a new member of the cytokine receptor family. Endocrinology 146:2354–2361

    Article  PubMed  CAS  Google Scholar 

  • Fukamachi S, Yada T, Mitani H (2005) Medaka receptors for somatolactin and growth hormone: phylogenetic paradox among fish growth hormone receptors. Genetics 171:1875–1883

    Article  PubMed  CAS  Google Scholar 

  • Funkenstein B, Cohen I (1996) Ontogeny of growth hormone protein and mRNA in the gilthead sea bream Sparus aurata. Growth Regul 6:16–21

    PubMed  CAS  Google Scholar 

  • Funkenstein B, Almuly R, Chan SJ (1997) Localization of IGF-I and IGF-I receptor mRNA in Sparus aurata larvae. Gen Comp Endocrinol 107:291–303

    Article  PubMed  CAS  Google Scholar 

  • Gevers EF, Milne J, Robinson ICAF, Loveridge N (1996) Single cell enzyme activity and proliferation in the growth plate: effects of growth hormone. J Bone Miner Res 11:1103–1111

    Article  PubMed  CAS  Google Scholar 

  • Gevers EF, Eerden BC van der, Karperien M, Raap AK, Robinson IC, Wit JM (2002) Localization and regulation of the growth hormone receptor and growth hormone-binding protein in the rat growth plate. J Bone Miner Res 17:1408–1419

    Article  PubMed  CAS  Google Scholar 

  • Gray ES, Tsai RW (1994) Characterization of striped bass growth hormone receptors by disulfide-bond reduction and cross-linking studies. J Exp Zool 268:428–435

    Article  PubMed  CAS  Google Scholar 

  • Guicheux J, Heymann D, Rousselle AV, Gouin F, Pilet P, Yamada S, Daculsi G (1998) Growth hormone stimulatory effects on osteoclastic resorption are partly mediated by insulin-like growth factor I: an in vitro study. Bone 22:25–31

    Article  PubMed  CAS  Google Scholar 

  • Hildahl J, Galay-Burgos M, Sweeney G, Einarsdóttir IE, Björnsson BTh (2007a) Identification of two isoforms of Atlantic halibut insulin-like growth factor-I receptor genes and quantitative gene expression during metamorphosis. Comp Biochem Physiol [B] 147:395–401

    Article  CAS  Google Scholar 

  • Hildahl J, Sweeney G, Galay-Burgos M, Einarsdóttir IE, Björnsson BTh (2007b) Cloning of Atlantic halibut growth hormone receptor genes and quantitative gene expression during metamorphosis. Gen Comp Endocrinol 151:143–152

    Article  PubMed  CAS  Google Scholar 

  • Huang H, Brown DD (2000) Overexpression of Xenopus laevis growth hormone stimulates growth of tadpoles and frogs. Proc Natl Acad Sci USA 97:190–194

    Article  PubMed  CAS  Google Scholar 

  • Inui Y, Miwa S (1985) Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol 60:450–454

    Article  PubMed  CAS  Google Scholar 

  • Jiao B, Huang X, Chan CB, Zhang L, Wang D, Cheng CH (2006) The co-existence of two growth hormone receptors in teleost fish and their differential signal transduction, tissue distribution and hormonal regulation of expression in seabream. J Mol Endocrinol 36:23–40

    Article  PubMed  CAS  Google Scholar 

  • Kopchick JJ, Andry JM (2000) Growth hormone (GH), GH receptor, and signal transduction. Mol Genet Metab 71:293–314

    Article  PubMed  CAS  Google Scholar 

  • Kuang YM, Li WS, Lin HR (2005) Molecular cloning and mRNA profile of insulin-like growth factor type-I receptor in orange-spotted grouper, Epinephelus coioides. Acta Biochim Biophys Sin (Shanghai) 37:327–334

    Article  CAS  Google Scholar 

  • Laiz-Carrion R, Mar Segura-Noguera M del, Pilar Martin del Rio M del, Mancera JM (2003) Ontogeny of adenohypophyseal cells in the pituitary of the American shad (Alosa sapidissima). Gen Comp Endocrinol 132:454–464

    Article  PubMed  CAS  Google Scholar 

  • Lewinson D, Shenzer P, Hochberg Z (1993) Growth hormone involvement in the regulation of tartrate-resistant acid phosphatase-positive cells that are active in cartilage and bone resorption. Calcif Tissue Int 52:216–221

    Article  PubMed  CAS  Google Scholar 

  • Li WS, Chen D, Wong AO, Lin HR (2005) Molecular cloning, tissue distribution, and ontogeny of mRNA expression of growth hormone in orange-spotted grouper (Epinephelus coioides). Gen Comp Endocrinol 144:78–89

    Article  PubMed  CAS  Google Scholar 

  • Li M, Raine JC, Leatherland JF (2007) Expression profiles of growth-related genes during the very early development of rainbow trout embryos reared at two incubation temperatures. Gen Comp Endocrinol 153:302–310

    Article  PubMed  CAS  Google Scholar 

  • Liao ZY, Zhu SQ (2004) Identification and characterization of GH receptor and serum GH-binding protein in Chinese sturgeon (Acipenser sinensis). Acta Biochim Biophys Sin (Shanghai) 36:811–816

    Article  CAS  Google Scholar 

  • Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A (2001) Roles of growth hormone and insulin-like growth factor-I in mouse postnatal growth. Dev Biol 229:141–162

    Article  PubMed  CAS  Google Scholar 

  • Ma X, Liu X, Zhang Y, Zhu P, Ye W, Lin H (2007) Two growth hormone receptors in Nile tilapia (Oreochromis niloticus): molecular characterization, tissue distribution and expression profiles in the gonad during the reproductive cycle. Comp Biochem Physiol [B] 147:325–339

    Article  CAS  Google Scholar 

  • Maures T, Chan SJ, Xu B, Sun H, Ding J, Duan C (2002) Structural, biochemical, and expression analysis of two distinct insulin-like growth factor I receptors and their ligands in zebrafish. Endocrinology 143:1858–1871

    Article  PubMed  CAS  Google Scholar 

  • Miwa S, Inui Y (1987) Effects of various doses of thyroxine and triiodothyronine on the metamorphosis of flounder (Paralichthys olivaceus). Gen Comp Endocrinol 67:356–363

    Article  PubMed  CAS  Google Scholar 

  • Miwa S, Yamano K, Inui Y (1992) Thyroid hormone stimulates gastric development in flounder larvae during metamorphosis. J Exp Zool 261:424–430

    Article  CAS  Google Scholar 

  • Mullis PE, Eble A, Marti U, Burgi U, Postel-Vinay MC (1999) Regulation of human growth hormone receptor gene transcription by triiodothyronine (T3). Mol Cell Endocrinol 147:17–25

    Article  PubMed  CAS  Google Scholar 

  • Nakao N, Tanaka M, Higashimoto Y, Nakashima K (2002) Molecular cloning, identification and characterization of four distinct receptor subtypes for insulin and IGF-I in Japanese flounder, Paralichthys olivaceus. J Endocrinol 173:365–375

    Article  PubMed  CAS  Google Scholar 

  • Nakao N, Higashimoto Y, Ohkubo T, Yoshizato H, Nakai N, Nakashima K, Tanaka M (2004) Characterization of structure and expression of the growth hormone receptor gene of the Japanese flounder (Paralichthys olivaceus). J Endocrinol 182:157–164

    Article  PubMed  CAS  Google Scholar 

  • Osse JWM, Van den Boogaart JGM (1997) Size of flatfish larvae at transformation, functional demands and historical constraints. J Sea Res 37:229–239

    Article  Google Scholar 

  • Otteson DC, Cirenza PF, Hitchcock PF (2002) Persistent neurogenesis in the teleost retina: evidence for regulation by the growth-hormone/insulin-like growth factor-I axis. Mech Dev 117:137–149

    Article  PubMed  CAS  Google Scholar 

  • Ozaki Y, Fukada H, Tanaka H, Kagawa H, Ohta H, Adachi S, Hara A, Yamauchi K (2006) Expression of growth hormone family and growth hormone receptor during early development in the Japanese eel (Anguilla japonica). Comp Biochem Physiol [B] 145:27–34

    Article  CAS  Google Scholar 

  • Pandolfi M, Paz DA, Maggese C, Ravaglia M, Vissio P (2001) Ontogeny of immunoreactive somatolactin, prolactin and growth hormone secretory cells in the developing pituitary gland of Cichlasoma dimerus (Teleostei, Perciformes). Anat Embryol (Berl) 203:461–468

    Article  CAS  Google Scholar 

  • Perrot V, Moiseeva EB, Gozes Y, Chan SJ, Ingleton P, Funkenstein B (1999) Ontogeny of the insulin-like growth factor system (IGF-I, IGF-II, and IGF-1R) in gilthead seabream (Sparus aurata): expression and cellular localization. Gen Comp Endocrinol 116:445–460

    Article  PubMed  CAS  Google Scholar 

  • Radaelli G, Domeneghini C, Arrighi S, Bosi G, Patruno M, Funkenstein B (2003) Localization of IGF-I, IGF-I receptor, and IGFBP-2 in developing Umbrina cirrosa (Pisces: Osteichthyes). Gen Comp Endocrinol 130:232–244

    Article  PubMed  CAS  Google Scholar 

  • Redruello B, Estevao MD, Rotllant J, Guerreiro PM, Anjos LI, Canario AV, Power DM (2005) Isolation and characterization of piscine osteonectin and downregulation of its expression by PTH-related protein. J Bone Miner Res 20:682–692

    Article  PubMed  CAS  Google Scholar 

  • Reinecke M, Björnsson BTh, Dickhoff WW, McCormick SD, Navarro 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 

  • Richardson NA, Anderson AJ, Rimmer MA, Sara VR (1995) Localization of insulin-like growth factor-I immunoreactivity in larval and juvenile barramundi (Lates calcarifer). Gen Comp Endocrinol 100:282–292

    Article  PubMed  CAS  Google Scholar 

  • Saele O, Solbakken JS, Watanabe K, Hamre K, Power D, Pittman K (2004) Staging of Atlantic halibut (Hippoglossus hippoglossus L.) from first feeding through metamorphosis, including cranial ossification independent of eye migration. Aquaculture 239:445–465

    Article  Google Scholar 

  • Saele O, Silva N, Pittman K (2006) Post-embryonic remodelling of neurocranial elements: a comparative study of normal versus abnormal eye migration in a flatfish, the Atlantic halibut. J Anat 209:31–41

    Article  PubMed  Google Scholar 

  • Saera-Vila A, Calduch-Giner JA, Perez-Sanchez J (2005) Duplication of growth hormone receptor (GHR) in fish genome: gene organization and transcriptional regulation of GHR type I and II in gilthead sea bream (Sparus aurata). Gen Comp Endocrinol 142:193–203

    Article  PubMed  CAS  Google Scholar 

  • Sanders EJ, Harvey S (2004) Growth hormone as an early embryonic growth and differentiation factor. Anat Embryol (Berl) 209:1–9

    Article  CAS  Google Scholar 

  • Schreiber AM (2001) Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): an osmoregulatory perspective. Comp Biochem Physiol [B] 129:587–595

    Article  CAS  Google Scholar 

  • Schreiber AM, Specker JL (1998) Metamorphosis in the summer flounder (Paralichthys dentatus): stage-specific developmental response to altered thyroid status. Gen Comp Endocrinol 111:156–166

    Article  PubMed  CAS  Google Scholar 

  • Schreiber AM, Specker JL (1999) Metamorphosis in the summer flounder, Paralichthys dentatus: thyroidal status influences salinity tolerance. J Exp Zool 284:414–424

    Article  PubMed  CAS  Google Scholar 

  • Solbakken JS, Norberg B, Watanabe K, Pittman K (1999) Thyroxine as a mediator of metamorphosis of Atlantic halibut, Hippoglossus hippoglossus. Environ Biol Fishes 56:53–65

    Article  Google Scholar 

  • Sun X, Zhu S, Chan SSH, Toresson G, Cheng CHK (1997) Identification and characterization of growth hormone receptors in snakehead fish (Ophiocephalus argus Cantor) liver. Gen Comp Endocrinol 108:374–385

    Article  PubMed  CAS  Google Scholar 

  • Tse DL, Tse MC, Chan CB, Deng L, Zhang WM, Lin HR, Cheng CH (2003) Seabream growth hormone receptor: molecular cloning and functional studies of the full-length cDNA, and tissue expression of two alternatively spliced forms. Biochim Biophys Acta 1625:64–76

    PubMed  CAS  Google Scholar 

  • Wargelius A, Fjelldal PG, Benedet S, Hansen T, Björnsson BTh, Nordgarden U (2005) A peak in GH-receptor expression is associated with growth activation in Atlantic salmon vertebrae, while upregulation of IGF-I receptor expression is related to increased bone density. Gen Comp Endocrinol 142:163–168

    Article  PubMed  CAS  Google Scholar 

  • Werther GA, Haynes KM, Barnard R, Waters MJ (1990) Visual demonstration of growth hormone receptors on human growth plate chondrocytes. J Clin Endocrinol Metab 70:1725–1731

    Article  PubMed  CAS  Google Scholar 

  • Yamano K, Miwa S (1998) Differential gene expression of thyroid hormone receptor alpha and beta in fish development. Gen Comp Endocrinol 109:75–85

    Article  PubMed  CAS  Google Scholar 

  • Yao K, Le Bail PY (1999) Biochemical characterization of growth hormone receptor in rainbow trout (Oncorhynchus mykiss) before and after purification. Fish Physiol Biochem 21:111–120

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Heiddis Smáradóttir, Arnar Jónsson, and Øystein Saele for larval sampling, and Nádia Silva for methodological assistance.

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Correspondence to Jon Hildahl.

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This work was carried out within the project “Arrested development: the molecular and endocrine basis of flatfish metamorphosis” (Q5RS-2002-01192) with financial support from the Commission of the European Communities. However, it does not necessarily reflect the Commission’s views and in no way anticipates its future policy in this area. This project was further supported by the Swedish Council for Agricultural and Forestry Research (FORMAS) and the Helge Ax:son Johnsons Foundation.

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Hildahl, J., Power, D.M., Björnsson, B.T. et al. Involvement of growth hormone-insulin-like growth factor I system in cranial remodeling during halibut metamorphosis as indicated by tissue- and stage-specific receptor gene expression and the presence of growth hormone receptor protein. Cell Tissue Res 332, 211–225 (2008). https://doi.org/10.1007/s00441-007-0568-2

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