Leptin and leptin receptor genes in Atlantic salmon: Cloning, phylogeny, tissue distribution and expression correlated to long-term feeding status

Abstract

The present study reports the complete coding sequences for two paralogues for leptin (sLepA1 and sLepA2) and leptin receptor (sLepR) in Atlantic salmon. The deduced 171-amino acid (aa) sequence of sLepA1 and 175 aa sequence for sLepA2 shows 71.6% identity to each other and clusters phylogenetically with teleost Lep type A, with 22.4% and 24.1% identity to human Lep. Both sLep proteins are predicted to consist of four helixes showing strong conservation of tertiary structure with other vertebrates. The highest mRNA levels for sLepA1 in fed fish (satiation ration=100%) were observed in the brain, white muscle, liver, and ovaries. In most tissues sLepA2 generally had a lower expression than sLepA1 except for the gastrointestinal tract (stomach and mid-gut) and kidney. Only one leptin receptor ortholog was identified and it shares 24.2% aa sequence similarity with human LepR, with stretches of highest sequence similarity corresponding to domains considered important for LepR signaling. The sLepR was abundantly expressed in the ovary, and was also high in the brain, pituitary, eye, gill, skin, visceral adipose tissue, belly flap, red muscle, kidney, and testis. Fish reared on a rationed feeding regime (60% of satiation) for 10 months grew less than control (100%) and tended to have a lower sLepA1 mRNA expression in the fat-depositing tissues visceral adipose tissue (p<0.05) and white muscle (n.s.). sLepA2 mRNA levels was very low in these tissues and feeding regime tended to affect its expression in an opposite manner. Expression in liver differed from that of the other tissues with a higher sLepA2 mRNA in the feed-rationed group (p<0.01). Plasma levels of sLep did not differ between fish fed restricted and full feeding regimes. No difference in brain sLepR mRNA levels was observed between fish fed reduced and full feeding regimes. This study in part supports that sLepA1 is involved in signaling the energy status in fat-depositing tissues in line with the mammalian model, whereas sLepA2 may possibly play important roles in the digestive tract and liver. At present, data on Lep in teleosts are too scarce to allow generalization about how the Lep system is influenced by tissue-specific energy status and, in turn, may regulate functions related to feed intake, growth, and adiposity in fish. In tetraploid species like Atlantic salmon, different Lep paralogues seems to serve different physiological roles.

Lack of leptin activity in blood samples of Adélie penguin and bar-tailed godwit

“…The well-characterized key role of mammalian leptin in the control of energy homeostasis appears to be only partially shared with leptins in non-mammalian vertebrates (Volkoff 2006, Ronnestad et al 2010. Leptin and LEPR in evolutionarily early vertebrates show relatively low sequence similarity as compared with their mammalian orthologs.…”

Long-term fasting in the anadromous Arctic charr is associated with down-regulation of metabolic enzyme activity and up-regulation of leptin A1 and SOCS expression in the liver.

“…Long-term fasting in the anadromous Arctic charr is associated with downregulation of metabolic enzyme activity and upregulation of leptin A1 and SOCS expression in the liver also supported by the presence of the Lep receptor (LepR) gene in this organ in several fish species Rønnestad et al, 2010;Tinoco et al, 2012;Trombley et al, 2012).…”

“…Mean ± s.e.m. hepatosomatic index (HSI; %), liver glycogen concentrations (µmolg been reported in Atlantic salmon (Rønnestad et al, 2010;Trombley et al, 2012), whereas a reduced liver Lep expression with fasting has been reported in goldfish (Carassius auratus) (Tinoco et al, 2012) and striped bass (Morone saxatilis) (Won et al, 2012), and no change with prolonged fasting in common carp (Cyprinus carpio) (Huising et al, 2006). The reason for these differences is not known, but they could relate to the degree of emaciation of the fish used in the different experiments, and interspecific differences in metabolic responses to an imposed fast.…”

“…In contrast to mammals, in which Lep is produced mainly in adipose tissue (Masuzaki et al, 1995), Lep is produced in numerous tissues in fish, including the liver (Wong et al, 2007;Kurokawa and Murashita, 2009;Rønnestad et al, 2010;Tinoco et al, 2012;Trombley et al, 2012). Hepatic LepA1 and LepA2 expression increased towards the end of a 7week period of feed restriction in Atlantic salmon (Salmo salar) (Trombley et al, 2012) and during the latter part of a 75day period of feed deprivation in Arctic charr (Frøiland et al, 2012).…”

Association study between single nucleotide polymorphisms in leptin and growth traits in Cyprinus carpio var. Jian

“…The first leptin-like gene was identified in the pufferfish (Takifugu rubripes) using syntenic gene analysis (Kurokawa et al, 2005). Leptin genes have subsequently been cloned from other teleost species, including common carp (Cyprinus carpio) (Huising et al, 2006), zebrafish (Danio rerio) (Gorissen et al, 2009), medaka (Oryzias latipes) (Kurokawa and Murashita, 2009), grass carp (Ctenopharyngodon idella) (Li et al, 2010), rainbow trout (Oncorhynchus mykiss) (Murashita et al, 2008), Atlantic salmon (Salmo salar) (Rønnestad et al, 2010;Angotzi et al, 2013), yellow catfish (Pelteobagrus fulvidraco) (Gong et al, 2013), orange-spotted grouper (Epinephelus coioides) , and Jian carp (Cyprinus carpio var. Jian) (Tang et al, 2013).…”