Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

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

  • 281 Accesses

  • 30 Citations

Abstract

The cellular sites of insulin-like growth factor I (IGF-I) synthesis in the early developing tilapia (0-140 days post fertilization, DPF) were investigated. IGF-I mRNA and peptide appeared in liver as early as 4 DPF and in gastro-intestinal epithelial cells between 5-9 DPF. In exocrine pancreas, the expression of IGF-I started at 4 DPF and continued until 90 DPF. IGF-I production was detected in islets at 6 DPF in non-insulin cells and occurred throughout life. In renal tubules and ducts, IGF-I production started at 8 DPF. IGF-I production in chondrocytes had its onset at 4 DPF, was more pronounced in growing regions and was also found in adults. IGF-I mRNA and peptide appeared in the cytoplasm of skeletal muscle cells at 4 DPF. In gill chloride cells, IGF-I production started at 6 DPF. At 13 DPF, IGF-I was detected in cardiac myocytes. IGF-I-producing epidermal cells appeared at 5 DPF. In brain and ganglia, IGF-I was expressed in virtually all neurones from 6 to 29 DPF, their number decreasing with age. Neurosecretory IGF-I-immunoreactive axons were first seen in the neurohypophysis around 17 DPF. Endocrine cells of the adenohypophysis exhibited IGF-I mRNA at 28 DPF and IGF-I immunoreactivity at 40 DPF. Thus, IGF-I appeared early (4-5 DPF), first in liver, the main source of endocrine IGF-I, and then in organs involved in growth or metabolism. The expression of IGF-I was more pronounced during development than in juvenile and adult life. Local IGF-I therefore seems to have a high functional impact in early growth, metabolism and organogenesis.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Ayson FG, Jesus EG de, 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

  2. Baños N, Moon TW, Castejon C, Gutiérrez J, Navarro I (1997) Insulin and insulin-like growth factor-I (IGF-I) binding in fish red muscle: regulation by high insulin levels. Regul Pept 68:181–187

  3. Baroiller JF, Desprez D, Carteret Y, Tacon P, Hoareau MC, Mélard C, Jalabert B (1997) Influence of environmental and social factors on the reproductive efficiency in three tilapia species, Oreochromis niloticus, O. aureus and the red tilapia (Red Florida strains). In: Fitzsimmons K (ed) Proceedings of the Fourth International Symposium on Tilapia in Aquaculture, 9-12 November 1997, Orlando, Fla., USA. Northeast Regional Agriculture Engineering Service, New York, pp 238–252

  4. Bern HA, McCormick SD, Kelley KM, Gray ES, Nishioka RS, Madsen SS, Tsai PL (1991) Insulin-like growth factors “under water”: role in growth and function of fish and other poikilothermic vertebrates. In: Spencer EM (ed) Modern concepts of insulin-like growth factors. Elsevier, New York, pp 85–96

  5. Berwert L, Segner H, Reinecke M (1995) Ontogeny of IGF-1 and the classical islet hormones in the turbot, Scophthalmus maximus. Peptides 16:113–122

  6. 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 135:324–323

  7. Caelers A, Schmid AC, Hrusovsky A, Reinecke M (2003) Insulin-like growth factor II mRNA is expressed in neurones of the brain of the bony fish Oreochromis mossambicus, the tilapia. Eur J Neurosci 18:355–363

  8. 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

  9. Castillo J, Codina M, Martinez ML, Navarro I, Gutiérrez J (2004) Metabolic and mitogenic effects of IGF-I and insulin on muscle cells of rainbow trout. Am J Physiol Regul Integr Comp Physiol 286:R935–R941

  10. Cheng CM, Cohen M, Tseng V, Bondy CA (2001) Endogenous IGF1 enhances cell survival in the postnatal dentate gyrus. J Neurosci Res 64:341–347

  11. Chourrout D, Itskovich J (1983) Three manipulations permitted by artificial insemination in tilapia: induced diploid gynogenesis, production of all triploid population and intergeneric hybridisation. In: Fishelson L, Yaron Z (eds) International Symposium on Tilapia in Aquaculture, Nazareth, Israel. Tel Aviv University, Tel Aviv, pp 246–255

  12. David I, Bosshard R, Kloas W, Reinecke M (2000) Insulin-like growth factor I in the anterior pituitary of the clawed frog Xenopus laevis: immunocytochemical and autoradiographic indication for a paracrine action and corelease with prolactin. J Neuroendocrinol 12:415–420

  13. Deane EE, Kelly SP, Collins PM, Woo NY (2003) Larval development of silver sea bream (Sparus sarba): ontogeny of RNA-DNA ratio, GH, IGF-I, and Na(+)-K(+)-ATPase. Mar Biotechnol (NY) 5:79–91

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

  15. 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

  16. 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 protein. Fish Physiol Biochem 11:371–379

  17. 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

  18. Duan CM, Inui Y (1990) Effects of recombinant eel growth hormone on the uptake of [35S]sulfate by ceratobranchial cartilages of the Japanese eel, Anguilla japonica. Gen Comp Endocrinol 79:320–325

  19. 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

  20. 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

  21. Edmondson SR, Thumiger SP, Werther GA, Wraight CJ (2003) Epidermal homeostasis: the role of the growth hormone and insulin-like growth factor systems. Endocr Rev 24:737–764

  22. Fryer JN (1979) A radioreceptor assay for purified teleost growth hormone. Gen Comp Endocrinol 39:123–130

  23. Funkenstein B, Silbergeld A, Cavari B, Laron Z (1989) Growth hormone increases plasma levels of insulin-like growth factor (IGF-I) in a teleost, the gilthead seabream (Sparus aurata). J Endocrinol 120:R19–R21

  24. 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

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

  26. Greene MW, Chen TT (1999) Quantitation of IGF-I, IGF-II, and multiple insulin receptor family member messenger RNAs during embryonic development in rainbow trout. Mol Reprod Dev 54:348–356

  27. Gutiérrez J, Parrizas M, Maestro MA, Navarro I, Plisetskaya EM (1995) Insulin and IGF-I binding and tyrosine kinase activity in fish heart. J Endocrinol 146:35–44

  28. Hansson H-A, Nilsson A, Isgaard J, Billig H, Isaksson O, Skottner A, Andersson IK, Rozell B (1988) Immunohistochemical localization of insulin-like growth factor I in the adult rat. Histochemistry 89:403–410

  29. Hirschberg R (1996) Insulin-like growth factor I in the kidney. Miner Electrolyte Metab 22:128–132

  30. Howarth GS (2003) Insulin-like growth factor-I and the gastrointestinal system: therapeutic indications and safety implications. J Nutr 133:2109–2112

  31. 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

  32. Jevdjovic T, Maake C, Eppler E, Zoidis E, Reinecke M, Zapf J (2004) Effects of insulin-like growth factor-I treatment on the endocrine pancreas of hypophysectomized rats: comparison with growth hormone replacement. Eur J Endocrinol 151:1–10

  33. Kakizawa S, Yamada K, Iino M, Watanabe M, Kano M (2003) Effects of insulin-like growth factor I on climbing fibre synapse elimination during cerebellar development. Eur J Neurosci 17:545–554

  34. Kelley KM, Gray ES, Siharath K, Nicoll CS, Bern HA (1993) Experimental diabetes mellitus in a teleost fish. II. Roles of insulin, growth hormone (GH), insulin-like growth factor-I, and hepatic GH receptors in diabetic growth inhibition in the goby, Gillichthys mirabilis. Endocrinology 132:2696–2702

  35. Koppang EO, Thomas GA, Ronningen K, Press CML (1998) Expression of insulin-like growth factor-I in the gastrointestinal tract of Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 18:167–175

  36. Leahy JL, Vandekerkhove KM (1990) Insulin-like growth factor-I at physiological concentrations is a potent inhibitor of insulin secretion. Endocrinology 126:1593–1598

  37. Leibush B, Parrizas M, Navarro I, Lappova Y, Maestro MA, Encinas M, Plisetskaya EM, Gutiérrez J (1996) Insulin and insulin-like growth factor-I receptors in fish brain. Peptides 61:155–161

  38. 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

  39. Madsen SS, Bern HA (1993) In-vitro effects of insulin-like growth factor-I on gill Na,K(+)-ATPase in coho salmon, Oncorhynchus kisutch. J Endocrinol 138:23–30

  40. Madsen SS, Jensen MK, Nhr J, Kristiansen K (1995) Expression of Na(+)-K(+)-ATPase in the brown trout, Salmo trutta: in vivo modulation by hormones and seawater. Am J Physiol 269:R1339–R1345

  41. Mancera JM, McCormick SD (1998) Evidence for growth hormone/insulin-like growth factor I axis regulation of seawater acclimation in the euryhaline teleost Fundulus heteroclitus. Gen Comp Endocrinol 111:103–112

  42. McCormick SD (1996) Effects of growth hormone and insulin-like growth factor I on salinity tolerance and gill Na, K+-ATPase in Atlantic salmon (Salmo salar): interaction with cortisol. Gen Comp Endocrinol 101:3–11

  43. McCormick SD, Tsai PI, Kelley KM, Nishioka RS, Bern HA (1992) Hormonal control of sulfate uptake by branchial cartilage of coho salmon: role of IGF-I. J Exp Zool 262:166–171

  44. Mendez E, Smith A, Figueiredo-Garutti ML, Planas JV, Navarro I, Gutiérrez J (2001) Receptors for insulin-like growth factor-I (IGF-I) predominate over insulin receptors in skeletal muscle throughout the life cycle of brown trout, Salmo trutta. Gen Comp Endocrinol 122:148–157

  45. Moon TW, Castejon C, Baños N, Maestro MA, Plisetskaya EM, Gutiérrez J, Navarro I (1996) Insulin and IGF-I binding in isolated trout cardiomyocytes. Gen Comp Endocrinol 103:264–272

  46. Moriyama S (1995) Increased plasma insulin-like growth factor-I (IGF-I) following oral and intraperitoneal administration of growth hormone to rainbow trout, Oncorhynchus mykiss. Growth Regul 5:164–167

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

  48. Ng TB, Leung TC, Cheng CHK, Woo NYS (1992) Growth hormone binding sites in tilapia (Oreochromis mossambicus) liver. Gen Comp Endocrinol 86:111–118

  49. Niblock MM, Brunso-Bechtold JK, Riddle DR (2000) Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci 20:4165–4176

  50. Niu PD, Pérez-Sanchez J, Le Bail PY (1993) Development of a protein binding assay for teleost insulin-like growth factor (IGF-like): relationship between growth hormone (GH) and IGF-like in the blood of rainbow trout (Oncorrhynchus mykiss). Fish Physiol Biochem 11:381–391

  51. 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

  52. Pierce AL, Fukada H, Dickhoff WW (2005) Metabolic hormones modulate the effect of growth hormone (GH) on insulin-like growth factor-I (IGF-I) mRNA level in primary culture of salmon hepatocytes. J Endocrinol 184:341–349

  53. Plisetskaya EM (1998) Some of my not so favorite things about insulin and insulin-like growth factors in fish. Comp Biochem Physiol [B] 121:3–11

  54. Plisetskaya EM, Bondareva VM, Duan C, Duguay SJ (1993) Does salmon brain produce insulin? Gen Comp Endocrinol 91:74–80

  55. Pozios KC, Ding J, Degger B, Upton Z, Duan C (2001) IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinase-signaling pathways. Am J Physiol Regul Integr Comp Physiol 280:R1230–R1239

  56. 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

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

  58. Reinecke M, Maake C, Falkmer S, Sara VR (1993) The branching of insulin-like growth factor 1 and insulin: an immunohistochemical analysis during phylogeny. Regul Pept 48:65–76

  59. 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

  60. Reinecke M, Schmid AC, Heyberger-Meyer B, Hunziker EB, Zapf J (2000) Effect of growth hormone and insulin-like growth factor I (IGF-I) on the expression of IGF-I mRNA and peptide in rat tibial growth plate and articular chondrocytes in vivo. Endocrinology 141:2847–2853

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

  62. 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

  63. 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

  64. Schmid AC, Naf E, Kloas W, Reinecke M (1999) Insulin-like growth factor-I and -II in the ovary of a bony fish, Oreochromis mossambicus, the tilapia: in situ hybridisation, immunohistochemical localisation, Northern blot and cDNA sequences. Mol Cell Endocrinol 156:141–149

  65. Schmid AC, Reinecke M, Kloas W (2000) Primary cultured hepatocytes of the bony fish, Oreochromis mossambicus, the tilapia: a valid tool for physiological studies on IGF-I expression in liver. J Endocrinol 166:265–273

  66. Schober DA, Simmen FA, Hadsell DL, Baumrucker CR (1990) Perinatal expression of type I IGF receptors in porcine small intestine. Endocrinology 126:1125–1132

  67. Segner H, Storch V, Reinecke M, Kloas W, Hanke W (1994) The development of functional digestive and metabolic organs in turbot, Scophthalmus maximus. Mar Biol 119:471–486

  68. Seidelin M, Madsen SS (1999) Endocrine control of Na,K+-ATPase and chloride cell development in brown trout (Salmo trutta): interaction of insulin-like growth factor-I with prolactin and growth hormone. J Endocrinol 162:127–135

  69. Seidelin M, Madsen SS, Byrialsen A, Kristiansen K (1999) Effects of insulin-like growth factor-I and cortisol on Na, K+-ATPase expression in osmoregulatory tissues of brown trout (Salmo trutta). Gen Comp Endocrinol 113:331–342

  70. Shamblott MJ, Chen TT (1993) Age-related and tissue-specific levels of five forms of insulin-like growth factor mRNA in a teleost. Mol Mar Biol Biotechnol 2:351–361

  71. Shamblott MJ, Cheng CM, Bolt D, Chen TT (1995) Appearance of insulin-like growth factor mRNA in the liver and pyloric ceca of a teleost in response to exogenous growth hormone. Proc Natl Acad Sci USA 92:6943–6946

  72. Shepherd BS, Sakamoto T, Nishioka RS, Richman NH, 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 USA 94:2068–2072

  73. Shved N, Berishvili G, D’Cotta H, Baroiller JF, Eppler E, Segner H, Reinecke M (2005) A survey on the expression of IGF-I in the early developing bony fish with special emphasis on the tilapia, Oreochromis niloticus. Ann N Y Acad Sci 1040:469–471

  74. Smith A, Chan SJ, Gutierrez J (2005) Autoradiographic and immunohistochemical localization of insulin-like growth factor-I receptor binding sites in brain of the brown trout, Salmo trutta. Gen Comp Endocrinol 141:203–213

  75. Steeb CB, Trahair JF, Tomas FM, Read LC (1994) Prolonged administration of IGF peptides enhances growth of gastrointestinal tissues in normal rats. Am J Physiol 266:G1090–G1098

  76. Tsai PI, Madsen SS, McCormick SD, Bern HA (1994) Endocrine control of cartilage in coho salmon: GH influence in vivo on the response to IGF-I in vitro. Zool Sci 11:299–303

  77. Van Schravendijk CF, Heylen L, Van den Brande JL, Pipeleers DG (1990) Direct effect of insulin and insulin-like growth factor-I on the secretory activity of rat pancreatic beta cells. Diabetologia 33:649–653

  78. 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

  79. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285

  80. 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

  81. Zhou X, Herman JP, Paden CM (1999) Evidence that IGF-I acts as an autocrine/paracrine growth factor in the magnocellular neurosecretory system: neuronal synthesis and induction of axonal sprouting. Exp Neurol 159:419–432

Download references

Author information

Correspondence to Manfred Reinecke.

Additional information

This study was supported by the SNF (NRP 50, project 4050-66580).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Berishvili, G., Shved, N., Eppler, E. et al. 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 (2006). https://doi.org/10.1007/s00441-005-0133-9

Download citation

Keywords

  • Liver
  • Gastro-intestinal tract
  • Pancreas
  • Kidney
  • Muscle
  • Brain
  • Pituitary
  • Gills
  • Heart
  • Epidermis
  • Tilapia