Cloning and tissue distribution of appetite‐regulating peptides in pirapitinga (Piaractus brachypomus)

Abstract

Pirapitinga (or red-bellied pacu, Piaractus brachypomus, Characiforme, Serrasalmidae) is an economically important South American fish for which the endocrine mechanism of the regulation of feeding has never been examined. To better understand these mechanisms, cDNAs encoding the appetite-regulating peptides orexin, cocaine- and amphetamine-regulated transcript (CART), apelin, cholecystokinin (CCK), peptide YY (PYY), leptin and ghrelin were isolated in pirapitinga and their mRNA distributions examined in peripheral tissues and brain. When compared to other fish, the sequences obtained for all peptides were most similar to those of other Characiforme fish (i.e. Mexican cavefish) and Siluriformes (catfish) as well as Cypriniformes (i.e. goldfish, zebrafish). All peptides were widely expressed within the brain. With the exception of CART, which was only expressed in brain, the mRNAs of all peptides were present in several peripheral tissues, including gastrointestinal tract, kidneys and gills. The widespread and peptide-specific distributions suggest that each peptide might have distinct physiological actions in the brain and on peripheral tissues, in particular on the gastrointestinal tract, which include feeding regulation. This preliminary study opens new avenues for further functional studies on the endocrine regulation of feeding in Serrasalmidae fish, including pirapitinga.

The Neuroendocrine Regulation of Food Intake in Fish: A Review of Current Knowledge

“…In several fish species, e.g., pirapitinga ( Piaractus brachypomus ) (Characiforme) (Volkoff, 2015a), cunner (Perciforme) (Hayes and Volkoff, 2014) and rainbow trout (Salmoniforme) (Varricchio et al, 2015), orexin mRNA/protein expression is high in the gastrointestinal tract, suggesting a role of the orexin system in regulating feeding and digestive processes. Among Perciformes, in Japanese sea perch ( Lateolabrax japonicus ), orexin-like ir is present in pituitary GH-containing cells, suggesting a control of growth by the orexin system (Suzuki et al, 2007) and in Cichlasoma dimerus , orexin-ir fibers are present in both hypothalamus and in pituitary, suggesting a neuroendocrine control of pituitary secretions (Pérez Sirkin et al, 2013).…”

“…Two CART isoforms have been identified in goldfish (Volkoff and Peter, 2001a) and common carp (Wan et al, 2012), and 4 in zebrafish (Akash et al, 2014) whereas, to date, only one form has been isolated for grass carp (Zhou et al, 2013; Liu et al, 2014), Characiformes [pirapitinga (serrasalmidae) (Volkoff, 2015a), pacu (serrasasalmidae) (Volkoff et al, 2017) and dourado (characidae) (Volkoff et al, 2016), red bellied piranha (serrasalmidae) (Volkoff, 2014a)], Salmoniformes [Atlantic salmon (Murashita et al, 2009a), rainbow trout (Figueiredo-Silva et al, 2012), Arctic charr (Striberny et al, 2015) and lake trout ( Salvelinus namaycush ) (Volkoff et al, 2007)], Siluriformes (channel catfish Kobayashi et al, 2008), Gadiformes (Atlantic cod Kehoe and Volkoff, 2007), Perciformes (cunner Babichuk and Volkoff, 2013), winter flounder (MacDonald and Volkoff, 2009a) and Atlantic halibut ( Hippoglossus hippoglossus ) (Gomes et al, 2015) (Pleuronectiformes), venomous toadfish Thalassophryne nattereri (Batrachoidiforme) (Magalhaes et al, 2006), rainbow smelt ( Osmerus mordax ) (Osmeriforme), pufferfishes ( Takifugu rubripes and Tetraodon nigroviridis , Tetraodontiforme) and stickleback Gasterosteus aculeatus (Gasterosteiforme) (cited in Murashita et al, 2009a). However, six forms of CART have been identified in the medaka (Beloniforme) (Murashita and Kurokawa, 2011) and seven forms in Senegalese sole Solea senegalensis (Pleuronectiforme), the highest number of CART genes reported to date in a vertebrate species (Bonacic et al, 2015).…”

“…The first direct evidence of the actions of CCK on feeding was provided by injections in goldfish (Himick and Peter, 1994), followed by cloning of goldfish CCK cDNA (Peyon et al, 1998) and the demonstration of periprandial variations in CCK mRNA expression levels (Peyon et al, 1999). Subsequently, a number of studies have characterized CCK in several fish, including other Cypriniformes (e.g., common carp Zhong et al, 2013; zebrafish Koven and Schulte, 2012; Tian et al, 2015; grass carp; blunt snout bream Ping et al, 2013; Ji et al, 2015), Characiformes (e.g., cavefish Wall and Volkoff, 2013, dourado Pereira et al, 2015; Volkoff et al, 2016, thin dogfish Oligosarcus hepsetus Vieira-Lopes et al, 2013, pirapitinga Volkoff, 2015a, red-bellied piranha Volkoff, 2014a, pacu Volkoff et al, 2017), Salmoniformes (e.g., Atlantic salmon Valen et al, 2011), Gadiformes (Atlantic cod Tillner et al, 2013), Perciformes [e.g., yellowtail (Furutani et al, 2013; Hosomi et al, 2014); Astatotilapia burtoni (Grone et al, 2012); cunner (Babichuk and Volkoff, 2013; Hayes and Volkoff, 2014); sea bass (Tillner et al, 2014); yellow croaker ( Larimichthys crocea ) (Cai et al, 2015); white sea bream, Diplodus sargus (Micale et al, 2012, 2014)], Pleuronectiformes (e.g., winter flounder (MacDonald and Volkoff, 2009a), Atlantic halibut Kamisaka et al, 2001, olive flounder Kurokawa et al, 2000) and Siluriformes (channel catfish Peterson et al, 2012). …”

Hypothalamic Integration of Metabolic, Endocrine, and Circadian Signals in Fish: Involvement in the Control of Food Intake

“…Orexins are present in numerous fish species with a broad distribution. Thus, orexin ir-cell bodies, preproorexin mRNA, and orexin proteins are abundant in hypothalamus and preoptic area of most species so far studied (Volkoff, 2015), areas associated with the control of food intake in fish.…”

Appetite-Controlling Endocrine Systems in Teleosts

“…Oral CCK administration inhibits feed intake in sea bass (201), while oral treatment with CCK antagonists increases food intake in rainbow trout (202). A single cck gene has been cloned in several teleost species, including yellowtail ( Seriola quinqueradiata ) (203), Atlantic herring ( Clupea harengus ) (204), and pirapitinga ( Piaractus brachypomus ) (205). However, two different cck sequences were identified in Japanese flounder ( Paralichthys olivaceus ), tetraodon (206), Atlantic salmon (207), and white sea bream ( Diplodus sargus ) (208), and three distinct cck genes exists in rainbow trout (209).…”