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

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.

Occurrence of ghrelin-producing cells, the ghrelin receptor and Na+,K+-ATPase in tissues of Atlantic halibut (Hippoglossus hippoglossus) during early development

“…GH might also act indirectly by stimulating hepatic insulin-like growth factor-I (IGF-I) production and secretion (for reviews, see Björnsson et al 2002;Reinecke 2010). IGF-I expression has also been detected in gills in adult tilapia (Reinecke et al 1997), striped bass (Tipsmark et al 2007) and Atlantic salmon (Tipsmark and Madsen 2009) and during the early development of tilapia (Berishvili et al 2006) and shi drum larvae (Radaelli et al 2003). Gill IGF-I is thought to have a paracrine/autocrine effect and extrahepatic IGF-I production might, with regard to hepatic production, be regulated by pituitary GH (for a review, see Reinecke 2010).…”

Ethinylestradiol differentially interferes with IGF-I in liver and extrahepatic sites during development of male and female bony fish

“…IGF-I seems to have a physiological impact on smoltification. The chloride cells of the filament epithelium not only express Na (McCormick 1996) but also in developing and adult fish IGF-I mRNA (Reinecke et al 1997, Radaelli et al 2003, Berishvili et al 2006a. In tilapia, the importance of local IGF-I expression is stressed by its very early appearance in chloride cells around 6-7 DPF (Berishvili et al 2006a).…”

“…The chloride cells of the filament epithelium not only express Na (McCormick 1996) but also in developing and adult fish IGF-I mRNA (Reinecke et al 1997, Radaelli et al 2003, Berishvili et al 2006a. In tilapia, the importance of local IGF-I expression is stressed by its very early appearance in chloride cells around 6-7 DPF (Berishvili et al 2006a). In several fish species, evidence has been presented that both circulating (liver-derived) IGF-I (Madsen & Bern 1993, Shepherd et al 1997, Inoue et al 2003 and autocrine/ paracrine IGF-I from the chloride cells (Sakamoto & Hirano 1993, Biga et al 2004) mediate the osmoregulatory actions of GH.…”

“…Sections were cut at 4 mm and processed for in situ hybridization using the sense (5 0 -GTCTGTGGAGAGCGAGGCTTT-3 0 ) and antisense (5 0 -AACCTTGGGTGCTCTTGGCATG-3 0 ) probes corresponding to the tilapia IGF-I B and E domains, as described (Schmid et al 1999, Berishvili et al 2006a. After dewaxing and rehydration, the sections were postfixed with 4% paraformaldehyde and 0 .…”

“…The organs studied included those of the central GH/IGF-I axis, i.e., pituitary and liver. Although fish liver is the major source of circulating IGF-I, IGF-I also occurs in extrahepatic sites (Reinecke et al 1997) where it is particularly expressed during development (Duguay et al 1996, Perrot et al 1999, Radaelli et al 2003, Berishvili et al 2006a. Thus, the alterations in IGF-I mRNA expression were also determined in organs showing high IGF-I expression during ontogeny, i.e., gills and brain.…”