Insulin-like growth factor (IGF) signalling and genome-wide transcriptional regulation in fast muscle of zebrafish following a single-satiating meal

Abstract

SUMMARY Male zebrafish (Danio rerio) were fasted for 7 days and fed to satiation over 3 h to investigate the transcriptional responses to a single meal. The intestinal content at satiety (6.3% body mass) decreased by 50% at 3 h and 95% at 9 h following food withdrawal. Phosphorylation of the insulin-like growth factor (IGF) signalling protein Akt peaked within 3 h of feeding and was highly correlated with gut fullness. Retained paralogues of IGF hormones genes were regulated with feeding, with igf1a showing a pronounced peak in expression after 3 h and igf2b after 6 h. Igf-I receptor transcripts were markedly elevated with fasting, and decreased to their lowest levels 45 min after feeding. igf1rb transcripts increased more quickly than igf1ra transcripts as the gut emptied. Paralogues of the insulin-like growth factor binding proteins (IGFBPs) were constitutively expressed, except for igfbp1a and igfbp1b transcripts, which were significantly elevated with fasting. Genome-wide transcriptional responses were analysed using the Agilent 44K oligonucleotide microarray and selected genes validated by qPCR. Fasting was associated with the upregulation of genes for the ubiquitin-proteasome degradation pathway, anti-proliferative and pro-apoptotic genes. Protein chaperones (unc45b, hspd1, hspa5, hsp90a.1, hsp90a.2) and chaperone interacting proteins (ahsa1 and stip1) were upregulated 3 h after feeding along with genes for the initiation of protein synthesis and mRNA processing. Transcripts for the enzyme ornithine decarboxylase 1 showed the largest increase with feeding (11.5-fold) and were positively correlated with gut fullness. This study demonstrates the fast nature of the transcriptional responses to a meal and provides evidence for differential regulation of retained paralogues of IGF signalling pathway genes.

Dynamic transcriptional regulation of autocrine/paracrine igfbp1, 2, 3, 4, 5, and 6 in the skeletal muscle of the fine flounder during different nutritional statuses

“…Igfbps regulate the half-life of circulating Igfs as well as modulating their availability and biological activity, either inhibiting or potentiating Igf 's actions depending on the EXP conditions, cell type, tissue, species, and physiological context (Wood et al 2000, Zhou et al 2004, Ning et al 2006, 2008, Ren et al 2008, Dai et al 2010, Amaral & Johnston 2011. Therefore, in the present work, the results were analyzed according to the physiological context of using two contrasting nutritional conditions: a catabolic period of fasting that leads to muscle atrophy followed by an anabolic period of refeeding that leads to hypertrophy of muscle.…”

“…Nevertheless, a recent report by Amaral & Johnston (2011) described that igfbp1 is expressed in skeletal muscle of zebra fish and is regulated by nutrition, increasing during fasting and rapidly returning to basal levels during refeeding. The fact that igfbp1 is upregulated during fasting has been associated with a negative role in growth in both fish and mammals (Maures & Duan 2002, Kajimura et al 2005, Kajimura & Duan 2007.…”

“…Previous studies on the biology of Igfbps in fish have shown that Igfbps regulate embryonic development (Duan et al 1999, Kajimura et al 2005) and exert ligand-dependent and -independent mechanisms (Dai et al 2010, Zhong et al 2011, as well as showing that Igfbps are modulated by Gh treatment (Duan et al 1999, Cheng et al 2002, Chen et al 2004, Pedroso et al 2009b, oxygen availability (Kajimura et al 2005, Rahman & Thomas 2011, Sun et al 2011, reproduction , Chen et al 2010, and nutrition , Bower et al 2008, Pedroso et al 2009a, Peterson & Waldbieser 2009, Amaral & Johnston 2011, Macqueen et al 2011. Nevertheless, studies on local muscle-derived igfbps (autocrine/ paracrine) have been scarce and have recently shown contrasting results, reflecting a complex physiology of Igfbps and suggesting that intricate patterns of regulation have evolved between and within teleost lineages , Bower et al 2008, Amaral & Johnston 2011, Macqueen et al 2011.…”

Experimental selection for body size at age modifies early-life history traits and muscle gene expression in adult zebrafish

“…cDNA at 40-fold dilution was used as the working solution. Primer pairs for the 15 known genes of the IGF system in the zebrafish (Amaral and Johnston, 2011) and myogenic regulatory factors (MRFs) were as described previously (Amaral and Johnston, 2012). Primers were designed to amplify the 'fecundity genes' (bmp15 and gdf9) and their receptors (bmpr1aa, bmpr1ab, bmpr1ba, bmpr1bb, bmpr2a, bmpr2b), and GH (gh1) and its receptors (ghra and ghrb) (Table1).…”

Alteration in expression of atrogenes and IGF-1 induced by fasting in Nile tilapia Oreochromis niloticus juveniles

“…Our results corroborate other reported findings with different fish species submitted to different fasting protocols. For instance, in rainbow trout juveniles, after 14 days of food deprivation the atrogin-1 levels increased and 12 h after refeeding decreased significantly (Seiliez et al 2008); in salmon white muscle, the expression of MuRF1 increased in fasted fish compared to fed control (Tacchi and Bicherdike 2012); and in Atlantic salmon and zebrafish, atrogin-1 and MuRF1 were also found to be upregulated during fasting and downregulated after refeeding (Bower et al 2009;Bower and Johnston 2010;Amaral and Johnston 2011).…”