Fish Physiology and Biochemistry

, Volume 22, Issue 2, pp 135–144

The involvement of growth hormone in growth regulation, energy homeostasis and immune function in the gilthead sea bream (Sparus aurata): a short review

  • J. Pérez-Sánchez
Article

Abstract

The aim of this mini-review is to provide a comprehensive survey of the physiological role of growth hormone (GH) in the Mediterranean sea bream (Sparus aurata). For this purpose, sea bream GH is now available as a recombinant and bioactive protein in a practically unlimited amount. In juvenile and adult fish, the liver is the most important target for the direct action of GH. Nevertheless, it must be noted that in sea bream larvae the greater concentration of GH-binding sites occurs in the head region, which also exhibits a fast growth. This finding suggests that GH exerts at this early stage of development a direct action on growing tissues rather than a systemic one mediated by hepatic IGF-I. However, the GH-liver axis is later a sensitive marker of growth performance, and seasonal changes in circulating GH levels and hepatic GH-binding are well characterized. The effect of age, water temperature and feeding regimes has also been studied. As a characteristic feature, fasting and malnourished fish show a decrease in hepatic GH-binding and circulating IGF-I, which increases pituitary GH release due to a lack of negative feedback inhibition. Interestingly, the up-regulation of plasma GH levels has also been described in fish fed to visual satiety. This, together with a decreased feed conversion, is more evident in fish fed high energy diets, and it has been suggested that this metabolic derangement is an adaptive response to protect adipose tissue and perhaps other organs and tissues from the excessive lipid deposition, when abundant energy is available. Experimental evidence also indicates that GH is able to exert a direct effect on sea bream erythroid and immunocytes. It is now recognized that GH receptors are present in erythroid, lymphoid and myeloid cells, and both GH and IGF-I have a mitogenic effect. GH also acts as a phagocytic-activating factor, and the presence of GH transcripts in the head kidney has been demonstrated by RT-PCR. All this provides suitable evidence for a pleiotropic and crucial role of GH in a lower vertebrate species such as sea bream.

fat deposition GH GH ontogeny IGF-I immune function nutrient regulation phagocytic cells proliferative role sea bream 

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References

  1. Abdel-Meguid, S.S., Shieh, H.S., Smith W.W., Dayringuer, H.E., Violand, B.N. and Bentle, L.A. 1987. Three-dimensional structure of genetically engineered variant of porcine growth hormone. Proc. Natl. Acad. Sci. USA 84: 6434–6437.Google Scholar
  2. Agellon, L.B. and Chen, T.T. 1986. Rainbow trout growth hormone: molecular cloning of cDNA and expression in E. coli. DNA 5: 463–471.Google Scholar
  3. Auperin, B., Baroiller, J.F., Ricordel, M.J., Fostier, A. and Prunet, P. 1997. Effect of confinement stress on circulating growth hormone and two prolactins in freshwater-adapted tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 108. 35–44.Google Scholar
  4. Badolato, F., Bond, H.M., Valerio, G., Petrella, A., Morrone, G. and Waters, M.J. 1994. Differential expression of surface membrane growth hormone receptor on human peripheral blood lymphocytes detected by dual fluorochrome flow cytometry. J. Clin. Endocrinol. Metabol. 79: 984–990.Google Scholar
  5. Ben-Atia, I., Fine, M., Tandler, A., Funkenstein, B., Maurice, S., Cavari, B. and Gertler, A. 1999. Preparation of recombinant gilthead sea bream (Sparus aurata) growth hormone and its use for stimulation of larvae growth by oral administration. Gen. Comp. Endocrinol. 113: 155–164.Google Scholar
  6. Besedovsky, H.O. and Del Rey, A. 1996. Immune-neuro-endocrine interactions: facts and hypothesis. Endocr. Rev. 17: 64–102.Google Scholar
  7. Boeuf, G. and Gaignon, J.J. 1989. Effects of rearing conditions on growth and thyroid hormones during smolting of Atlantic salmon Salmo salar. Aquaculture 82: 29–38.Google Scholar
  8. Calduch-Giner, J.A. and 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.Google Scholar
  9. Calduch-Giner, J.A., Pendón, C., Valdivia, M.M. and Pérez-Sánchez, J. 1998. Recombinant somatolactin as a stable and bioactive protein in a cell culture bioassay: development and validation of a sensitive and reproducible radioimmunoasay. J. Endocrinol. 156: 441–447.Google Scholar
  10. Calduch-Giner, J.A., Sitjà-Bobadilla, A., Alvarez-Pellitero, P. and Pérez-Sánchez J. 1995. Evidence for a direct action of GH on haemopoietic cells of a marine fish, the gilthead sea bream (Sparus aurata). J. Endocrinol. 146: 459–467.Google Scholar
  11. Calduch-Giner, J.A., Sitjà-Bobadilla, A., Alvarez-Pellitero, P. and Pérez-Sánchez, J. 1997. Growth hormone as an in vitro phagocyte-activating factor in the gilthead sea bream (Sparus aurata L.). Cell Tiss. Res. 287: 535–540.Google Scholar
  12. Cambre, M., Mareels, G., Corneille, S., Moons, L., Ollevier, F. and Vandesande, F. 1990. Chronological appearance of the different hypophysial hormones in the pituitary of sea bass larvae (Dicentrarchus labrax) during their early development: and immunocytochemical demonstration. Gen. Comp. Endocrinol. 77: 408–415.Google Scholar
  13. Cao, Q-P., Duguay, S.J., Plisetskaya, E., Steiner, D.F. and Chan S.J. 1989. Nucleotide sequence and growth hormone regulated expression of salmon insulin-like growth factor-I mRNA. Mol. Endocrinol. 3: 2005–2010.Google Scholar
  14. Cerdá-Reverter, J.M., Zanuy, S., Carrillo, M. and Kah, O. 1996. Development of enzyme immunoassays for 3,5,3'-triiodo-L-thyronine and L-thyroxine: time-course studies on the effect of food deprivation on plasma thyroid hormones in two marine teleosts, sea bass (Dicentrarchus labrax L.) and sea bream (Sparus aurata L.). Gen. Comp. Endocrinol. 103: 290–300.Google Scholar
  15. Chang, J.P. and De Leeuw, R. 1990. In vitro goldfish growth hormone responses to gonadotropin-releasing hormone: possible roles of extracellular calcium and arachidonic acid metabolism. Gen. Comp. Endocrinol. 80: 155–164.Google Scholar
  16. Chang, J.P., Jobin, R.M. and De Leeuw, R. 1991. Possible involvement of protein kinase C in gonadotropin and growth hormone release from dispersed goldfish pituitary cells. Gen. Comp. Endocrinol. 81: 447–463.Google Scholar
  17. Company, R., Calduch-Giner, J.A., Kaushik, S. and Pérez-Sánchez, J. 1999a. Growth performance and adiposity in gilthead sea bream (Sparus aurata): risks and benefits of high energy diets. Aquaculture 171: 279–292.Google Scholar
  18. Company, R., Calduch-Giner, J.A., Pérez-Sánchez, J. and Kaushik, S. 1999b. Protein sparing effect of dietary lipids in common dentex (Dentex dentex): a comparative study with sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax). Aquat. Living Resour. 12: 23–30.Google Scholar
  19. Cunningham, B.C. and Wells, J.A. 1989. High-resolution epitope maping in hGH-receptor interactions by alanine-scaning mutagenesis. Science 244: 1081–1084.Google Scholar
  20. Dauncey, M.J. 1995. From whole body to molecule: an integrated approach to the regulation of metabolism and growth. Thermochimica Acta 250: 305–318.Google Scholar
  21. Dickhoff, W.W., Beckman, B.R., Larsen, D.A., Duan, C. and Moriyama, S. 1997. The role of growth in endocrine regulation of salmon smoltification. Fish Physiol. Biochem. 17: 231–236.Google Scholar
  22. Duan, C. 1998. Nutritional and developmental regulation of insulin-like growth factors in fish. J. Nutrit. 128: 306S–314S.Google Scholar
  23. Duan, C., Plisetskaya, E. and Dickhoff, W. 1995. Expression of insulin-like growth factor I in normally and abnormally developing coho salmon (Oncorhynchus kisutch). Endocrinology 136: 446–452.Google Scholar
  24. Duguay, S.J., Lai-Zhang, J., Steiner, D.F., Funkenstein, B. and Chan, S.J. 1996. Development and tissue-regulated expression of IGF-I and IGF-II mRNAs in Sparus aurata. J. Mol. Endocrinol. 16: 123–132.Google Scholar
  25. Edwards, C.K., Ghiasuddin, S.M., Shepper, J.M., Yunger, L.M. and Kelley, K.M. 1988. A newly defined property of somatotropin: priming of macrophages for production of superoxide anion. Science 239: 769–771.Google Scholar
  26. Farbridge, K.J. and Leatherland, J.F. 1992. Plasma growth hormone levels in fed and fasted rainbow trout (Oncorhynchus mykiss) are decreased following handling stress. Fish Physiol. Biochem. 10: 67–73.Google Scholar
  27. Funkenstein, B., Almuly, R. and Chan, S.J. 1997. Localization of IGF-I and IGF-I receptor mRNA in Sparus aurata larvae. Gen. Comp. Endocrinol. 107: 291–303.Google Scholar
  28. Funkenstein, B., Tandler, A. and Cavari, B. 1992. Developmental expression of the growth hormone gene in the gilthead sea bream Sparus aurata. Mol. Cell. Endocrinol. 87: R7–R9.Google Scholar
  29. Giustina, A. and Wehernberg, W.B. 1992. The role of glucocorticoids in the regulation of growth hormone secretion. Mechanisms and clinical significance. Trends Endocrinol. Metab. 3: 309–311.Google Scholar
  30. Golde, D.W., Bersh, N. and Li, C.H. 1978. Growth hormone: species specific stimulation of erythropoiesis in vitro. Science 196: 1112–1113.Google Scholar
  31. Gomez, J.M., Boujard, T., Boeuf, G., Solari, A. and Le Bail, P-Y. 1997. Individual nycthemeral plasma profiles of thyroid hormones in rainbow trout (Oncorhynchus mykiss) in relation with cortisol, growth hormone and growth rate. Gen. Comp. Endocrinol. 107: 74–83.Google Scholar
  32. Kao, T.L., Harbour, D.V. and Meyer, W.J. 1992. Immunoreactive growth hormone production by cultured lymphocytes. Ann. NY Acad. Sci. 650: 179–181.Google Scholar
  33. Kawauchi, H. and Yasuda, A. 1989. Evolutionary aspects of growth hormones from non mammalian species. In: Advances in Growth Hormones and Growth Factor Research. pp. 51–68. Edited by E.E. Muller, D. Cochi and V. Locatelli. Pythagora Press, Berlin.Google Scholar
  34. Kelly, K.W. 1989. Growth hormone lymphocytes and macrophages. Biochem. Pharmacol. 38: 705–713.Google Scholar
  35. Kiess, W. and Butenandt, O. 1985. Specific growth hormone receptors on human peripheral mononuclear cells: reexpression, identification, and characterization. J. Clin. Endocrinol. Metab. 60: 740–746.Google Scholar
  36. Kim, J.D., Näntö-Salonen, K., Szcepankiewich, J.R., Rosenfeld, R.G. and Glasscock, G.F. 1993. Evidence for pituitary regulation of somatic growth, insulin-like growth factors-I and II, and their binding protein in the fetal growth. Pedr. Res. 33: 144–151.Google Scholar
  37. Kitlen, J.W., Hejbøl, E.K., Zinck, T., Varming, K., Byatt, J.C. and McLean, E. 1997. Growth performance and respiratory burst activity in rainbow trout treated with growth hormone and vaccine. Fish & Shellfish Immunol. 7: 297–304.Google Scholar
  38. Le Bail, P.Y., Mourot, B., Zohar, Y. and Pérez-Sánchez, J. 1993a. Application of a sensitive radioimmunoassay for the measurement of growth hormone in gilthead sea bream, Sparus aurata, and other sparid fish. Can. J. Zool. 71: 1500–1505.Google Scholar
  39. Le Bail, P-Y., Pérez-Sánchez, J., Yao, K. and Maisse, G. 1993b. Effect of GH treatment on salmonid growth: study of the variability of response. In: Aquaculture: Fundamental and Applied Research, pp. 173–197. Edited by B. Lahlou and P. Vitiello. American Geophysical Union, Washington, DC.Google Scholar
  40. Mackenzie, D.S., Van Putte, C.M. and Leiner, K.A. 1998. Nutrient regulation of endocrine function in fish. Aquaculture 161: 3–25.Google Scholar
  41. Marchant, T.A. and Peter, R.E. 1986. Seasonal variations in body growth rates and circulating levels of growth hormone in the goldfish, Carassius auratus. J. Exp. Zool. 237: 231–239.Google Scholar
  42. Martial, J.A., Seeberg, P.H., Guenzi, D. and Goodman, H.M. 1979. Human growth hormone: complementary DNA cloning and expression in bacteria. Science 205: 602–607.Google Scholar
  43. Martínez-Barberá, J.P., Pendón, C., Rodríguez, R., Pérez-Sánchez, J. and Valdivia M.M. 1994. Cloning, expression, and characterization of a recombinant gilthead sea bream growth hormone. Gen. Comp. Endocrinol. 96: 179–188.Google Scholar
  44. Martínez-Barberá, J.P., Vila, V., Valdivia, M.M. and Castrillo, J.L. 1997 Molecular cloning of gilthead seabream (Sparus auratus) pituitary transcription factor GHF-1/Pit-1. Gene 185: 87–93.Google Scholar
  45. Martí-Palanca, H. and Pérez-Sánchez, J. 1994. Developmental regulation of growth hormone binding in the gilthead sea bream, Sparus aurata. Growth Reg. 4: 14–19.Google Scholar
  46. Martí-Palanca, H., Martínez-Barberá, J.P., Pendón, C., Valdivia, M.M., Pérez-Sánchez, J. and Kaushik, S. 1996. Growth hormone as a function of age and dietary protein:energy ratio in a marine teleost, the gilthead sea bream (Sparus aurata). Growth Reg. 6: 253–259.Google Scholar
  47. Matthews, L.S., Hammer, R.E., Brinster, R.L. and Palmiter, R.D. 1988. Expression of insulin-like growth factor-I in transgenic mice with elevated levels of growth hormone is correlated with growth. Endocrinology 123: 433–437.Google Scholar
  48. Merchav, S., Tatarsky, I. and Hochberg, Z. 1988. Enhancement of human granulopoiesis in vitro by biosynthetic insulin-like growth factor-I/somatomedin C and human growth hormone. J. Clin. Invest. 81: 791–797.Google Scholar
  49. Muñoz, P., Calduch-Giner, J.A., Sitjà-Bobadilla, A., Alvarez-Pellitero, P. and Pérez-Sánchez, J. 1998. Modulation of the respiratory burst activity of Mediterranean sea bass (Dicentrarchus labrax L.) phagocytes by growth hormone and parasitic status. Fish & Shellfish Immunol. 8: 25–36.Google Scholar
  50. Murphy,W.J., Durum. S.K., Anver, M., Frazier, M. and Longo, D.L. 1992. Recombinant human growth hormone promotes human lymphocyte engraftment in immunodeficient mice and results in an increased incidence of human Epstein Barr virus-induced B-cell lymphoma. Brain Behav. Immunol. 6: 355–364.Google Scholar
  51. Ono, M. and Takayama, Y. 1992. Stuctures of cDNAs encoding chum salmon pituitary-specific transcription factor, Pit-1/GHF-1. Gene 116: 275–279.Google Scholar
  52. Palmiter, R.D., Norstedt, G., Gelinas, R.E., Hammer, R.E. and Brinster, R.L. 1983. Metallothionein-human GH fusion genes stimulates growth of mice. Science 222: 809–814.Google Scholar
  53. Pendón, C., Martínez-Barberá, J.P., Pérez-Sánchez, J., Rodríguez, R.B., Grenett, H. and Valdivia, M.M. 1994. Cloning of the sole (Solea senegalensis) growth hormone-Gene 145: 237–240Google Scholar
  54. Peng, C. and Peter, R.E. 1997. Neuroendocrine regulation of growth hormone secretion and growth in fish. Zool. Studies 36: 79–89.Google Scholar
  55. Pérez-Sánchez, J. and Le Bail, P-Y. 1999. Growth hormone axis as marker of nutritional status and growth performance in fish. Aquaculture 177: 117–128.Google Scholar
  56. Pérez-Sánchez, J., Martí-Palanca, H. and Kaushik, S. 1995. Ration size and protein intake affect circulating growth hormone concentration, hepatic growth hormone binding and plasma insulinlike growth factor-I immunoreactivity in a marine teleost, the gilthead sea bream (Sparus aurata). J. Nutrit. 125: 546–552.Google Scholar
  57. Pérez-Sánchez, J., Martí-Palanca, H. and Le Bail P-Y. 1994a. Homologous growth hormone (GH) binding in gilthead sea bream (Sparus aurata). Effect of fasting and refeeding on hepatic GH-binding and plasma somatomedin-like immunoreactivity. J. Fish Biol. 44: 287–301.Google Scholar
  58. Pérez-Sánchez, J., Martí-Palanca, H. and Le Bail, P-Y. 1994b. Seasonal changes in circulating growth hormone (GH), hepatic GH-binding and plasma insulin-like growth factor-I immunoreactivity in a marine fish, gilthead sera bream, Sparus aurata. Fish Physiol. Biochem. 13: 199–208.Google Scholar
  59. Pérez-Sánchez, J., Smal, J. and Le Bail, P-Y. 1991. Location and characterization of growth hormone binding sites in the central nervous system of a teleost fish (Oncorhynchus mykiss). Growth Reg. 1: 145–152.Google Scholar
  60. Pérez-Sánchez, J., Weil, C. and Le Bail, P-Y. 1992. Effects of human insulin-like growth factor-I on release of growth hormone by rainbow trout (Oncorhynchus mykiss) pituitary cells. J. Exp. Zool. 262: 287–290.Google Scholar
  61. Pickering, A.D., Pottinger, T.G., Sumpter, J.P., Carragher, J.F. and Le Bail, P-Y. 1991. Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 83: 86–93.Google Scholar
  62. Power, D.M. and Canario, A.V.M. 1992. Immunocytochemistry of somatotrophs, gonadotrophs, prolactin and adrenocorticotropin cells in larval sea bream (Sparus auratus) pituitaries. Cell Tiss. Res. 269: 341–346.Google Scholar
  63. Power, D.M., Canario, A.V.M. and Ingleton, P.M. 1996. Somatotropin release-inhibiting factor and galanin innervation in the hypothalamus and pituitaryu of seabream (Sparus aurata). Gen. Comp. Endocrinol. 101: 264–274.Google Scholar
  64. Ricordel, M-J., Smal, J. and Le Bail, P-Y. 1995. Application of a recombinant cichlid growth hormone radioimmunoassay to measure native GH in tilapia (Oreochromis niloticus) bred at different temperatures. Aquat. Living Resour. 8: 153–160.Google Scholar
  65. Sakai, M., Kobayashi, M. and Kawauchi, H. 1995. Enhancement of chemiluminiscent responses of phagocytic cells from rainbow trout, Oncorhynchus mykiss, by injection of growth hormone. Fish & Shellfish Immunol. 5: 375–379.Google Scholar
  66. Sakai, M., Kobayashi, M. and Kawauchi, H. 1996a. Mitogenic effects of growth hormone and prolactin on chum salmon, Onchorhynchus keta, leukocytes in vitro. Vet. Immunol. Immunopathol. 53: 185–189.Google Scholar
  67. Sakai, M., Kobayashi, M. and Kawauchi, H. 1996b. In vitro activation of fish phagocytic cells by GH, prolactin and somatolactin. J. Endocrinol. 151: 113–118.Google Scholar
  68. Scanes, C.G. 1997. Ontogeny of the hypothalamic-pituitary (growth hormone)-insulin-like growth factor-I axis in birds. Am. Zool. 37: 524–535.Google Scholar
  69. Sitjà-Bobadilla, A. and Pérez-Sánchez, J. 1999. Diet related changes in non-specific immune response of European sea bass (Dicentrarchus labrax L.). Fish & Shellfish Immunol. (In press.)Google Scholar
  70. Storebakken, T., Hung, S.S.O., Calvert, C.C. and Plisetskaya, E. 1991. Nutrient partitioning in rainbow trout at different feeding rates. Aquaculture 96: 191–203.Google Scholar
  71. Theill, L.E. and Karin, M. 1993. Transcriptional control of GH expression and anterior piruitary development. Endocrine Rev. 14: 670–689.Google Scholar
  72. Thommes, R.C., Woods, J.E., Aramburo, C., Buonomo, F.C. and Scanes C.G. 1992. Effects of surgical decapitation and chicken growth hormone (cGH) replacement theraphy on chick embrionyc growth. Growth Devel. Aging 56: 167–178.Google Scholar
  73. Toguyeni, A., Baroiller, J.F., Fostier, A., Le Bail, P-Y., Kuhn, E.R., Mol, K.A. and Fauconneau, B. 1996. Consequences of food restriction on short-term growth variation and on plasma circulating hormones in Oreochromis niloticus in relation to sex. Gen. Comp. Endocrinol. 103: 167–175.Google Scholar
  74. Vandeputte, M. 1990. Contribution a l'Etude de l'Endocrinologie de la Croissance aux Premiers Stages du Development Chez la Truite Comune. D.E.A. Biologie et Agronomie, Universite de Rennes I.Google Scholar
  75. Warwich-Davies, J., Lowrie, D.B., and Cole, P.J. 1995. Growth hormone is a human macrophage activating factor. Priming of human monocytes for enhanced release of H2O2. J. Immunol. 154: 1909–1918.Google Scholar
  76. Weigent, D.A. 1996. Immunoregulatory properties of growth hormone and prolactin. Pharmacol. Ther. 69: 237–257.Google Scholar
  77. Weigent, D.A. and Blalock, J.E. 1994. Effect of the administration of growth-hormone producing lymphocytes on weight gain and immune function in dwarf mice. Neuroimmunomodulation 1: 50–58.Google Scholar
  78. Wendelaar Bonga, S.E. 1997. The stress response in fish. Physiol. Rev. 77: 591–625.Google Scholar
  79. Yamada, S., Hata, J. and Yamashita, S. 1993. Molecular cloning of fish Pit-1 cDNA and its functional binding to promoter of gene expressed in the pituitary. J. Biol. Chem. 268: 24631–24366.Google Scholar
  80. Yamaguchi, K., Yasuda, A., Kishida, M., Hirano, T., Sano, H. and Kawauchi, H. 1987. Primary structure of eel (Anguilla japonica) growth hormone. Gen. Comp. Endocrinol. 66: 447–453.Google Scholar
  81. Yao, K., Niu, P.D., Le Gac, F. and Le Bail, P-Y. 1991. Presence of specific growth hormone binding sites in rainbow trout (Onchorhynchus mykiss) tissues: characterization of the hepatic receptor. Gen. Comp. Endocrinol. 81: 72–82.Google Scholar

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© Kluwer Academic Publishers 2000

Authors and Affiliations

  • J. Pérez-Sánchez
    • 1
  1. 1.Instituto de Acuicultura de Torre de la Sal (CSIC)CastellónSpain

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