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

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.

Exploring the larval transcriptome of the common sole (Solea solea L.)

“…In the Atlantic halibut, the GH-IGFI system is established at the start of autonomous feeding [59]. In the common sole, GHRH and GH display similar expression patterns, with a significant up-regulation before metamorphosis onset (6 dph, soon after mouth opening), followed by a decrease in mRNA levels until 24 dph and a then subsequent increase (albeit not significant) at 33 dph.…”

Regulation of growth hormone (GH) receptor (GHR1 and GHR2) mRNA level by GH and metabolic hormones in primary cultured tilapia hepatocytes

“…Conserved synteny indicates that both teleost GHR clades are orthologous with tetrapod GHRs, and the identification of the Coho salmon GHR1 clade receptor as an SLR led to the hypothesis that teleost GHR1 clade receptors are SLRs [18,20,47]. Consistent with this idea, GHR1 clade receptors are highly expressed in the skin [1,25,47], and a recent study showed that skin expression levels of a GHR1 clade receptor are increased by adaptation to a black background in a South American cichlid [7]. However, several studies have not supported an interaction of SL with teleost GHR1 clade receptors.…”

Metamorphosis in Teleosts

“…Cellular proliferation in the suborbital tissue of one side of the cranium may “push” one eye across the dorsal midline (Bao et al, 2011). Whether this proliferation is stimulated by TH directly or whether intermediary signals are involved remains unknown, but GH and IGF pathways likely serve as more proximal factors (Hildahl et al, 2008). In several flatfish mutants, cranial asymmetry is decoupled from internal organ asymmetry, suggesting that the two are regulated by independent mechanisms (Hashimoto et al, 2002).…”