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Growth hormone expression in ontogenic development in gilthead sea bream

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Abstract

The pattern of expression of the growth hormone (GH) gene was studied during the early development of gilthead sea bream (Sparus aurata). The GH transcript was detected from the 2nd day of the larval stage onwards. In the next stages the expression level fluctuated, possibly due to different regulatory factors. The distribution of GH mRNA studied by in situ hybridization (ISH) was found to be pituitary specific. Hybridization signals for GH mRNA were detected for the first time in 4-day-old larvae. Throughout development the cells that express GH mRNA were mainly located in the proximal pars distalis. Mammosomatotroph cells coexpressing GH and PRL were not detected in juveniles or adults. Moreover, the possible involvement of GH in asynchronic growth in cultivation of gilthead sea bream was also examined by ISH. No differences in the distribution of GH cells were observed in the three sizes of juveniles of gilthead sea bream studied. These results suggest that the transcription of GH is involved in the early developmental stages of sea bream and the asynchronous growth-related changes are not due to distinct distribution of GH cells.

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References

  • Arakawa E, Kaneko T, Tsukamoto K, Hirano T (1992) Immunocytochemical detection of prolactin and growth hormone cells in the pituitary during early development of the Japanese eel, Anguilla japonica. Zool Sci 9:1061–1066

    CAS  Google Scholar 

  • Astola A, Pendón C, Ortíz M, Valdivia MM (1996) Cloning and expression of somatolactin, a pituitary hormone related to growth hormone and prolactin from gilthead seabream, Sparus aurata. Gen Comp Endocrinol 104:330–336

    Article  CAS  PubMed  Google Scholar 

  • Ayson FG, Kaneko T, Hasegawa S, Hirano T (1994) Differential expression of two prolactin and growth hormone genes during early development of tilapia (Oreochromis mossambicus) in fresh water and seawater: implications for possible involvement in osmoregulation during early life stages. Gen Comp Endocrinol 95:143–152

    Article  CAS  PubMed  Google Scholar 

  • Balon EK (1981) Saltatory processes and altricial to precocial forms in the ontogeny of fishes. Am Zool 21:573–596

    Google Scholar 

  • Borrelli E (1994) Pitfalls during development: controlling differentiation of the pituitary gland. Trends Genet 10:222–224

    Article  CAS  PubMed  Google Scholar 

  • Calduch-Giner JA, Pérez-Sánchez J (1999) Expression of growth hormone (GH) gene in the head kidney of gilthead sea bream (Sparus aurata). J Exp Zool 283:326–330

    Article  CAS  Google Scholar 

  • Cambré ML, Mareels G, Corneillie S, Moons L, Ollevier F, Vandesande F (1990) Chronological appearance of the different hypophysial hormones in the pituitary of sea bass larvae (Dicentrarchus labrax) during their early development: an immunocytochemical demonstration. Gen Comp Endocrinol 77:408–415

    CAS  PubMed  Google Scholar 

  • Cavari B, Funkenstein B, Kawauchi H (2000) Cloning of a second variant of somatolactin-encoding cDNA from the gilthead seabream Sparus aurata. Fish Physiol Biochem 22:145–150

    CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    CAS  PubMed  Google Scholar 

  • Dorshkind K, Horseman ND (2000) The roles of prolactin, growth hormone, insulin-like growth factor-I, and thyroid hormones in lymphocyte development and function: insights from genetic models of hormone and hormone receptor deficiency. Endocr Rev 21:292–312

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Funkenstein B, Chen TT, Powers DA, Cavari B (1991) Cloning and sequencing of the gilthead seabream (Sparus aurata) growth hormone-encoding cDNA. Gene 103:243–247

    CAS  PubMed  Google Scholar 

  • Funkenstein B, Tandler A, Cavari B (1992) Developmental expression of the growth hormone gene in the gilthead sea bream Sparus aurata. Mol Cell Endocrinol 87:7–9

    Google Scholar 

  • Funkenstein B, Kawauchi H, Cavari B (1997) Ontogeny of somatolactin mRNA in the gilthead sea bream Sparus aurata. Fish Physiol Biochem 17:247–252

    Article  CAS  Google Scholar 

  • García-Hernández MP, García-Ayala A, Elbal MT, Agulleiro B (1996) The adenohypophysis of Mediterranean yellowtail, Seriola dumerilii (Risso, 1810): an immunocytochemical study. Tissue Cell 28:577–585

    PubMed  Google Scholar 

  • Greene MW, Chen TT (1997) Temporal expression pattern of insulin-like growth factor mRNA during embryonic development in a teleostei, rainbow trout (Oncorhynchus mykiss). Mol Mar Biol Biotechnol 6:144–151

    CAS  PubMed  Google Scholar 

  • Harvey S, Johnson CDM, Sharma P, Sanders EJ, Hull KL (1998) Growth hormone: a paracrine growth factor in embryonic development? Comp Biochem Physiol 119C:305–315

    Google Scholar 

  • Harvey S, Johnson CD, Sanders EJ (2000) Extra-pituitary growth hormone in peripheral tissues of early chick embryos. J Endocrinol 166:489–502

    CAS  PubMed  Google Scholar 

  • Herrero-Turrión MJ, Velasco A, Rodríguez RE, Aijón J, Lara JM (2002) Co-expression of somatolactin mRNAs in the pituitary gland of gilthead sea bream. Anat Embryol 205:407–416

    Article  PubMed  Google Scholar 

  • Herrero-Turrión MJ, Rodríguez RE, Aijón J, Lara JM (2003a) Transient expression pattern of prolactin in Sparus aurata. J Mol Endocrinol 31:69–84

    Google Scholar 

  • Herrero-Turrión MJ, Rodríguez RE, Velasco A, Aijón J, Lara JM (2003b) Differential expression and cellular localization of somatolactin-1 and -2 during early development in the gilthead sea bream. Gen Comp Endocrinol 132:77–87

    Google Scholar 

  • Huang L, Specker JL (1994) Growth hormone- and prolactin-producing cells in the pituitary gland of striped bass (Morone saxatilis): immunocytochemical characterization at different life stages. Gen Comp Endocrinol 94:225–236

    Article  CAS  PubMed  Google Scholar 

  • LeGac F, Blaise O, Fostier A, LeBail P-Y, Loir M, Mourot B, Weil C (1993) Growth hormone (GH) and reproduction: a review. Fish Physiol Biochem 11:219–232

    CAS  Google Scholar 

  • Llewellyn L, Ramsurn VP, Sweeney GE, Wigham T, Santos CR, Power DM (1995) Cloning and characterisation of a fish aldolase B gene. Biochim Biophys Acta 1263:75–78

    Article  CAS  PubMed  Google Scholar 

  • Mal AO, Swanson P, Dickhoff WW (1989) Immunocytochemistry of the developing salmon pituitary gland. Am Zool 29:94A

    Google Scholar 

  • Martí-Palanca H, Pérez-Sánchez J (1994) Development regulation of the growth hormone binding in the gilthead sea bream, Sparus aurata. Growth Regul 4:14–19

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Murphy AE, Harvey S (2001) Extrapituitary betaTSH and GH in early chick embryos. Mol Cell Endocrinol 185:161–171

    Article  CAS  PubMed  Google Scholar 

  • Naito N, Takahashi A, Nakai Y, Kawauchi H, Hirano T (1983) Immunocytochemical identification of the prolactin-secreting cells in the teleost pituitary with an antiserum to chum salmon prolactin. Gen Comp Endocrinol 50:282–291

    CAS  PubMed  Google Scholar 

  • Naito N, de Jesus EG, Nakai Y, Hirano T (1993) Ontogeny of pituitary cell-types and the hypothalamo-hypophysial relationship during early development of chum salmon, Oncorhynchus keta. Cell Tissue Res 272:429–437

    Google Scholar 

  • Nicoll CS, Mayer GL, Rusell SM (1986) Structural features of prolactins and growth hormones that can be related to their biological properties. Endocr Rev 7:169–203

    CAS  PubMed  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 203:461–468

    CAS  PubMed  Google Scholar 

  • Parhar IS, Iwata M, Pfaff DW, Schwanzel-Fukuda M (1995) Embryonic development of gonadotropin-releasing hormone neurons in the sockeye salmon. J Comp Neurol 362:256–270

    CAS  PubMed  Google Scholar 

  • Peng C, Peter RE (1997) Neuroendocrine regulation of growth hormone secretion and growth fish. Zool Studies 36:79–89

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Perrot V, Moiseeva EB, Gozes Y, Chan SJ, Funkenstein B (2000) Insulin-like growth factor receptors and their ligands in gonads of a hermaphroditic species, the gilthead seabream (Sparus aurata): expression and cellular localization. Biol Reprod 63:229–241

    CAS  PubMed  Google Scholar 

  • Pérez-Sánchez J (2000) The involvement of growth hormone in growth regulation, energy homeostasis and immune function in the gilthead sea bream (Sparus aurata): a short review. Fish Physiol Biochem 22:135–144

    Article  Google Scholar 

  • Peter RE, Marchant TA (1995) The endocrinology of growth in carp and related species. Aquaculture 129:299–321

    Article  CAS  Google Scholar 

  • Popper DM, Golden O, Shezifi Y (1992) Size distribution of juvenile gilthead sea bream (Sparus aurata), practical aspects. Isr J Aquacult-Bamid 44:147–187

    Google Scholar 

  • Power DM, Canario AV (1992) Immunocytochemistry of somatotrophs, gonadotrophs, prolactin and adrenocorticotropin cells in larval sea bream (Sparus auratus) pituitaries. Cell Tissue Res 269:341–346

    CAS  PubMed  Google Scholar 

  • Quesada J, Lozano MT, Ortega A, Agulleiro B (1988) Immunocytochemical and ultrastructural characterization of the cell types in the adenohypophysis of Sparus aurata L. (teleost). Gen Comp Endocrinol 72:209–225

    CAS  PubMed  Google Scholar 

  • Ramesh R, Kuenzel WJ, Buntin JD, Proudman JA (2000) Identification of growth-hormone- and prolactin-containing neurons within the avian brain. Cell Tissue Res 299:371–383

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rendón C, Rodríguez-Gómez FJ, Muñoz-Cueto JA, Piñuela C, Sarasquete C (1997) An immunocytochemical study of pituitary cells of the Senegalese sole, Solea senegalensis (Kaup 1858). Histochem J 29:813–822

    PubMed  Google Scholar 

  • Ruijter JM (1987) Development and aging of the teleost pituitary: qualitative and quantitative observations in the annual cyprinodont Cynolebias whitei. Anat Embryol 175:379–386

    CAS  PubMed  Google Scholar 

  • Saga T, Oota Y, Nozaki M, Swanson P (1993) Salmonid pituitary gonadotrophs. III. Chronological appearance of GTH I and other adenohypophysial hormones in the pituitary of the developing rainbow trout (Oncorhynchus mykiss irideus). Gen Comp Endocrinol 92:233–241

    Article  CAS  PubMed  Google Scholar 

  • Saga T, Yamaki K, Doi Y, Yoshizuka M (1999) Chronological study of the appearance of adenohypophysial cells in the ayu (Plecoglossus altivelis). Anat Embryol 200:469–475

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Shepherd BS, Madsen SS, Nishioka RS, Siharath K, Richman NH3, Bern HA, Grau EG (1997) Osmoregulatory actions of growth hormone and prolactin in an advanced teleost. Gen Comp Endocrinol 106:95–101

    Article  CAS  PubMed  Google Scholar 

  • Santos CR, Brinca L, Ingleton PM, Power DM (1999) Cloning, expression, and tissue localisation of prolactin in adult sea bream (Sparus aurata). Gen Comp Endocrinol 114:57–66

    Article  CAS  PubMed  Google Scholar 

  • Shepherd BS, Sakamoto T, Nishioka RS, Richman NH3, Mori I, Madsen SS, Chen TT, Hirano T, Bern HA, Grau EG (1997) Somatotropic actions of the homologous growth hormone and prolactins in the euryhaline teleost, the tilapia, Oreochromis mossambicus. Proc Natl Acad Sci U S A 94:2068–2072

    Article  CAS  PubMed  Google Scholar 

  • Takayama Y, Ono M, Rand-Weaver M, Kawauchi H (1991) Greater conservation of somatolactin, a presumed pituitary hormone of the growth hormone/prolactin family than of growth hormone in teleost fish. Gen Comp Endocrinol 83:366–374

    CAS  PubMed  Google Scholar 

  • Toubeau G, Poilve A, Baras E, Nonclercq D, De Moor S, Beckers JF, Dessy-Doize C, Heuson-Stiennon JA (1991) Immunocytochemical study of cell type distribution in the pituitary of Barbus barbus (Teleostei, Cyprinidae). Gen Comp Endocrinol 83:35–47

    CAS  PubMed  Google Scholar 

  • Villaplana M, García-Ayala A, Chaves-Pozo E, Agulleiro B (2000) Identification of mammosomatotropes, growth hormone cells and prolactin cells in the pituitary gland of the gilthead sea bream (Sparus aurata L., Teleostei) using light immunocytochemical methods: an ontogenic study. Anat Embryol 202:421–429

    CAS  PubMed  Google Scholar 

  • Volckaert FAM, Mugoyo JWM, Lescroart O, Grisez L, Ollevier F (1999) Immunohistochemically detected ontogeny of prolactin and growth hormone cells in the African catfish Clarias gariepinus. Comp Biochem Physiol 122B:423–431

    CAS  Google Scholar 

  • Voss JW, Rosenfeld MG (1992) Anterior pituitary development: short tales from dwarf mice. Cell 70:527–530

    CAS  PubMed  Google Scholar 

  • Yan HY, Thomas P (1991) Histochemical and immunocytochemical identification of the pituitary cell types in three sciaenid fishes: Atlantic croaker (Micropogonias undulatus), spotted seatrout (Cynoscion nebulosus), and red drum (Sciaenops ocellatus). Gen Comp Endocrinol 84:389–400

    CAS  PubMed  Google Scholar 

  • Yang BY, Greene M, Chen TT (1999) Early embryonic expression of the growth hormone family protein genes in the developing rainbow trout, Oncorhynchus mykiss. Mol Reprod Dev 53:127–134

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank G.H. Jenkins for revising the English version of this manuscript, M.T. Sánchez for technical assistance and Mariscos de Estero, S.A. (Ayamonte, Huelva, Spain), for providing the fish used in this study.

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Correspondence to J. M. Lara.

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This work was supported by the FISS PI021730, Junta de Castilla y León SA067/03 and BOS2000-1119 projects.

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Herrero-Turrión, M.J., Rodríguez, R.E., Velasco, A. et al. Growth hormone expression in ontogenic development in gilthead sea bream. Cell Tissue Res 313, 81–91 (2003). https://doi.org/10.1007/s00441-003-0735-z

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  • DOI: https://doi.org/10.1007/s00441-003-0735-z

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