Neuropeptide Y and melanocortin receptors in fish: regulators of energy homeostasis

Arends RJ, Vermeer H, Martens GJM, Leunissen JAM, Bonga SEW, Flik G (1998) Cloning and expression of two proopiomelanocortin mRNAs in the common carp (Cyprinus carpio). Mol Cell Endocrinol 143:23–31 Aspiras AC, Rohner N, Martineau B, Borowsky RL, Tabin CJ (2015) Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions. Proc Natl Acad Sci USA 112:9668–9673 Bjarnadottir TK, Gloriam DE, Hellstrand SH, Kristiansson H, Fredriksson R, Schioth HB (2006) Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 88:263–273 Blomqvist AG, Söderberg C, Lundell I, Milner RJ, Larhammar D (1992) Strong evolutionary conservation of neuropeptide Y: sequences of chicken, goldfish, and Torpedo marmorata DNA clones. Proc Natl Acad Sci USA 89:2350–2354 Bockaert J, Pin JP (1999) Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 18:1723–1729 Boyce-Derricott J, Nagler JJ, Cloud JG (2009) Regulation of hepatic estrogen receptor isoform mRNA expression in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 161:73–78 Butler AA, Kesterson RA, Khong K, Cullen MJ, Pelleymounter MA, Dekoning J, Baetscher M, Cone RD (2000) A unique metabolic syndrome causes obesity in the melanocortin-3 receptor-deficient mouse. Endocrinology 141:3518–3521 Butler AA, Girardet C, Mavrikaki M, Trevaskis JL, Macarthur H, Marks DL, Farr SA (2017) A life without hunger: the ups (and downs) to modulating melanocortin-3 receptor signaling. Front Neurosci 11:128 Cerda-Reverter JM, Schioth HB, Peter RE (2003) The central melanocortin system regulates food intake in goldfish. Regul Pept 115:101–113 Cerdá-Reverter JM, Larhammar D (2000) cNeuropeptide Y family of peptides: structure, anatomical expression, function, and molecular evolution. Biochem Cell Biol 78:371–392 Chen AS, Marsh DJ, Trumbauer ME, Frazier EG, Guan XM, Yu H, Rosenblum CI, Vongs A, Feng Y, Cao L, Metzger JM, Strack AM, Camacho RE, Mellin TN, Nunes CN, Min W, Fisher J, Gopal-Truter S, MacIntyre DE, Chen HY et al (2000) Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat Genet 26:97–102 Chhajlani V (1996) Distribution of cDNA for melanocortin receptor subtypes in human tissues. Biochem Mol Biol Int 38:73–80 Cone RD (2005) Anatomy and regulation of the central melanocortin system. Nat Neurosci 8:571–578 Cone RD (2006) Studies on the physiological functions of the melanocortin system. Endocr Rev 27:736–749 de Pedro N, López-Patino MA, Guijarro AI, Pinillos ML, Delgado MJ, Alonso-Bedate M (2000) NPY receptors and opioidergic system are involved in NPY-induced feeding in goldfish. Peptides 21:1495–1502 de Pedro N, Martinez-Alvarez R, Delgado MJ (2006) Acute and chronic leptin reduces food intake and body weight in goldfish (Carassius auratus). J Endocrinol 188:513–520 Demski LS (2012) The neural control of feeding in elasmobranchs: a review and working model. Environ Biol Fishes 95:169–183 Dores RM, Lecaude S (2005) Trends in the evolution of the proopiomelanocortin gene. Gen Comp Endocrinol 142:81–93 Dorsam RT, Gutkind JS (2007) G-protein-coupled receptors and cancer. Nat Rev Cancer 7:79–94 Duarte-Neves J, de Almeida LP, Cavadas C (2016) Neuropeptide Y (NPY) as a therapeutic target for neurodegenerative diseases. Neurobiol Dis 95:210–224 Fällmar H, Sundström G, Lundell I, Mohell N, Larhammar D (2011) Neuropeptide Y/peptide YY receptor Y2 duplicate in zebrafish with unique introns displays distinct peptide binding properties. Comp Biochem Phys B 160:166–173 Fan ZC, Sartin JL, Tao YX (2008) Pharmacological analyses of two naturally occurring porcine melanocortin-4 receptor mutations in domestic pigs. Domest Anim Endocrinol 34:383–390 Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 63:1256–1272 Fredriksson R, Larson ET, Yan YL, Postlethwait JH, Larhammar D (2004) Novel neuropeptide Y Y2-like receptor subtype in zebrafish and frogs supports early vertebrate chromosome duplications. J Mol Evol 58:106–114 Gantz I, Fong TM (2003) The melanocortin system. Am J Physiol 284:E468–E474 Gantz I, Konda Y, Tashiro T, Shimoto Y, Miwa H, Munzert G, Watson SJ, DelValle J, Yamada T (1993) Molecular cloning of a novel melanocortin receptor. J Biol Chem 268:8246–8250 Ghamari-Langroudi M, Cakir I, Lippert RN, Sweeney P, Litt MJ, Ellacott KLJ, Cone RD (2018) Regulation of energy rheostasis by the melanocortin-3 receptor. Sci Adv 4:eaat0866 Hinney A, Volckmar AL, Knoll N (2013) Melanocortin-4 receptor in energy homeostasis and obesity pathogenesis. Prog Mol Biol Transl 114:147–191 Hoegg S, Brinkmann H, Taylor JS, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203 Holzer P, Reichmann F, Farzi A (2012) Neuropeptide Y, peptide YY and pancreatic polypeptide in the gut–brain axis. Neuropeptides 46:261–274 Hoskins LJ, Volkoff H (2012) The comparative endocrinology of feeding in fish: insights and challenges. Gen Comp Endocrinol 176:327–335 Hughes DA, Hinney A, Brumm H, Wermter AK, Biebermann H, Hebebrand J, Stoneking M (2009) Increased constraints on MC4R during primate and human evolution. Hum Genet 124:633–647 Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, Berkemeier LR, Gu W, Kesterson RA, Boston BA, Cone RD, Smith FJ, Campfield LA, Burn P, Lee F (1997) Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88:131–141 Jegou S, Boutelet I, Vaudry H (2000) Melanocortin-3 receptor mRNA expression in pro-opiomelanocortin neurones of the rat arcuate nucleus. J Neuroendocrinol 12:501–505 Kalananthan T, Lai F, Gomes AS, Murashita K, Handeland S, Rønnestad I (2020) The melanocortin system in Atlantic salmon (Salmo salar L.) and its role in appetite control. Front Neuroanat 14:48 Kim KS, Larsen N, Short T, Plastow G, Rothschild MF (2000) A missense variant of the porcine melanocortin-4 receptor (MC4R) gene is associated with fatness, growth, and feed intake traits. Mamm Genome 11:131–135 Kim KS, Reecy JM, Hsu WH, Anderson LL, Rothschild MF (2004) Functional and phylogenetic analyses of a melanocortin-4 receptor mutation in domestic pigs. Domest Anim Endocrinol 26:75–86 Kishi T, Aschkenasi CJ, Lee CE, Mountjoy KG, Saper CB, Elmquist JK (2003) Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J Comp Neurol 457:213–235 Kitahara N, Nishizawa T, Iida K, Okazaki H, Andoh T, Soma GI (1988) Absence of a gamma-melanocyte-stimulating hormone sequence in proopiomelanocortin mRNA of chum salmon Oncorhynchus keta. Comp Biochem Physiol B 91:365–370 Klovins J, Haitina T, Ringholm A, Löwgren M, Fridmanis D, Slaidina M, Stier S, Schiöth HB (2004) Cloning of two melanocortin (MC) receptors in spiny dogfish: MC3 receptor in cartilaginous fish shows high affinity to ACTH-derived peptides while it has lower preference to γ-MSH. Eur J Biochem 271:4320–4331 Larhammar D (1996) Evolution of neuropeptide Y, peptide YY and pancreatic polypeptide. Regul Pept 62:1–11 Larhammar D, Wraith A, Berglund MM, Holmberg SKS, Lundell I (2001) Origins of the many NPY-family receptors in mammals. Peptides 22:295–307 Larson ET, Fredriksson R, Johansson SRT, Larhammar D (2003) Cloning, pharmacology, and distribution of the neuropeptide Y-receptor Yb in rainbow trout. Peptides 24:385–395 Larsson TA, Olsson F, SundstrÖm G, Brenner S, Venkatesh B, Larhammar D (2005) Pufferfish and zebrafish have five distinct NPY receptor subtypes, but have lost appetite receptors Y1 and Y5. Ann NY Acad Sci 1040:375–377 Larsson A, Larson ET, Fredriksson R, Conlon JM, Larhammar D (2006) Characterization of NPY receptor subtypes Y2 and Y7 in rainbow trout Oncorhynchus mykiss. Peptides 27:1320–1327 Lee YS, Poh LK, Loke KY (2002) A novel melanocortin 3 receptor gene (MC3R) mutation associated with severe obesity. J Clin Endocrinol Metab 87:1423–1426 Li JT, Yang Z, Chen HP, Zhu CH, Deng SP, Li GL, Tao YX (2016) Molecular cloning, tissue distribution, and pharmacological characterization of melanocortin-4 receptor in spotted scat, Scatophagus argus. Gen Comp Endocrinol 230–231:143–152 Li L, Yang Z, Zhang YP, He S, Liang XF, Tao YX (2017) Molecular cloning, tissue distribution, and pharmacological characterization of melanocortin-4 receptor in grass carp (Ctenopharyngodon idella). Domest Anim Endocrinol 59:140–151 Logan DW, Bryson-Richardson RJ, Taylor MS, Currie P, Jackson IJ (2003a) Sequence characterization of teleost fish melanocortin receptors. Ann NY Acad Sci 994:319–330 Logan DW, Bryson-Richardson RJ, Pagan KE, Taylor MS, Currie PD, Jackson IJ (2003b) The structure and evolution of the melanocortin and MCH receptors in fish and mammals. Genomics 81:184–191 Lotta LA, Mokrosiński J, de Oliveira EM, Li C, Sharp SJ, Luan J, Brouwers B, Ayinampudi V, Bowker N, Kerrison N (2019) Human gain-of-function MC4R variants show signaling bias and protect against obesity. Cell 177(597–607):e599 Lundell I, Blomqvist AG, Berglund MM, Schober DA, Johnson DG, Statnick MA, Gadski RA, Gehlert DR, Larhammar D (1995) Cloning of a human receptor of the NPY receptor family with high affinity for pancreatic polypeptide and peptide YY. J Biol Chem 270:29123–29128 Lundell I, Berglund MM, Starbäck P, Salaneck E, Gehlert DR, Larhammar D (1997) Cloning and characterization of a novel neuropeptide Y receptor subtype in the zebrafish. DNA Cell Biol 16:1357–1363 Martemyanov KA, Garcia-Marcos M (2018) Making useful gadgets with miniaturized G proteins. J Biol Chem 293:7474–7475 Matsuda K, Kang KS, Sakashita A, Yahashi S, Vaudry H (2011) Behavioral effect of neuropeptides related to feeding regulation in fish. Ann NY Acad Sci 1220:117–126 Metz JR, Peters JJM, Flik G (2006) Molecular biology and physiology of the melanocortin system in fish: a review. Gen Comp Endocrinol 148:150–162 Michel MC, Beck-Sickinger A, Cox H, Doods HN, Herzog H, Larhammar D, Quirion R, Schwartz T, Westfall T (1998) XVI. International union of pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacol Rev 50:143–150 Miller WE, Lefkowitz RJ (2001) Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr Opin Cell Biol 13:139–145 Morton G, Cummings D, Baskin D, Barsh G, Schwartz M (2006) Central nervous system control of food intake and body weight. Nature 443:289 Mountjoy KG, Mortrud MT, Low MJ, Simerly RB, Cone RD (1994) Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol 8:1298–1308 Narnaware YK, Peter RE (2001a) Effects of food deprivation and refeeding on neuropeptide Y (NPY) mRNA levels in goldfish. Comp Biochem Physiol B 129:633–637 Narnaware YK, Peter RE (2001b) Neuropeptide Y stimulates food consumption through multiple receptors in goldfish. Physiol Behav 74:185–190 Narnaware YK, Peyon PP, Lin X, Peter RE (2000) Regulation of food intake by neuropeptide Y in goldfish. Am J Physiol Regul Integr Comp Physiol 279:R1025–R1034 Ni XP, Butler AA, Cone RD, Humphreys MH (2006) Central receptors mediating the cardiovascular actions of melanocyte stimulating hormones. J Hypertens 24:2239–2246 Offermanns S (2003) G-proteins as transducers in transmembrane signalling. Prog Biophys Mol Biol 83:101–130 Oldham WM, Hamm HE (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat Rev Mol Cell Biol 9:60–71 Rao YZ, Chen R, Zhang Y, Tao YX (2019) Orange-spotted grouper melanocortin-4 receptor: modulation of signaling by MRAP2. Gen Comp Endocrinol 284:113234 Reichmann F, Holzer P (2016) Neuropeptide Y: a stressful review. Neuropeptides 55:99–109 Ritter SL, Hall RA (2009) Fine-tuning of GPCR activity by receptor-interacting proteins. Nat Rev Mol Cell Biol 10:819–830 Rodrigues AR, Almeida H, Gouveia AM (2015) Intracellular signaling mechanisms of the melanocortin receptors: current state of the art. Cell Mol Life Sci 72:1331–1345 Rønnestad I, Gomes AS, Murashita K, Angotzi R, Jönsson E, Volkoff H (2017) Appetite-controlling endocrine systems in teleosts. Front Endocrinol 8:73 Salaneck E, Fredriksson R, Larson ET, Conlon JM, Larhammar D (2001) A neuropeptide Y receptor Y1-subfamily gene from an agnathan, the European river lamprey: a potential ancestral gene. Eur J Biochem 268:6146–6154 Salaneck E, Larsson TA, Larson ET, Larhammar D (2008) Birth and death of neuropeptide Y receptor genes in relation to the teleost fish tetraploidization. Gene 409:61–71 Sawyer TK, Sanfilippo PJ, Hruby VJ, Engel MH, Heward CB, Burnett JB, Hadley ME (1980) 4-Norleucine, 7-D-phenylalanine-a-melanocyte-stimulating hormone: a highly potent a-melanotropin with ultralong biological activity. Proc Natl Acad Sci USA 77:5754–5758 Schjolden J, Schiöth HB, Larhammar D, Winberg S, Larson ET (2009) Melanocortin peptides affect the motivation to feed in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 160:134–138 Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661–671 Sebhat IK, Martin WJ, Ye Z, Barakat K, Mosley RT, Johnston DB, Bakshi R, Palucki B, Weinberg DH, MacNeil T, Kalyani RN, Tang R, Stearns RA, Miller RR, Tamvakopoulos C, Strack AM, McGowan E, Cashen DE, Drisko JE, Hom GJ et al (2002) Design and pharmacology of N-[(3R)-1,2,3,4-tetrahydroisoquinolinium- 3-ylcarbonyl]-(1R)-1-(4-chlorobenzyl)- 2-[4-cyclohexyl-4-(1H–1,2,4-triazol- 1-ylmethyl)piperidin-1-yl]-2-oxoethylamine (1), a potent, selective, melanocortin subtype-4 receptor agonist. J Med Chem 45:4589–4593 Sharma P, Arvidsson AK, Wraith A, Beck-Sickinger AG, Jönsson-Rylander AC, Larhammar D (1999) Characterization of the cloned Atlantic cod neuropeptide Y-Yb receptor: peptide-binding requirements distinct from known mammalian Y receptors. Gen Comp Endocrinol 115:422–428 Silva AP, Xapelli S, Grouzmann E, Cavadas C (2005) The putative neuroprotective role of neuropeptide Y in the central nervous system. Curr Drug Targets CNS Neurol Disord 4:331–347 Silverstein JT, Plisetskaya EM (2000) The effects of NPY and insulin on food intake regulation in fish. Am Zool 40:296–308 Silverstein JT, Breininger J, Baskin DG, Plisetskaya EM (1998) Neuropeptide Y-like gene expression in the salmon brain increases with fasting. Gen Comp Endocrinol 110:157–165 Smith AI, Funder JW (1988) Proopiomelanocortin processing in the pituitary, central nervous system, and peripheral tissues. Endocr Rev 9:159–179 Srinivasan S, Lubrano-Berthelier C, Govaerts C, Picard F, Santiago P, Conklin BR, Vaisse C (2004) Constitutive activity of the melanocortin-4 receptor is maintained by its N-terminal domain and plays a role in energy homeostasis in humans. J Clin Invest 114:1158–1164 Staubert C, Tarnow P, Brumm H, Pitra C, Gudermann T, Gruters A, Schoneberg T, Biebermann H, Rompler H (2007) Evolutionary aspects in evaluating mutations in the melanocortin 4 receptor. Endocrinology 148:4642–4648 Sundström G, Larsson TA, Xu B, Heldin J, Larhammar D (2013) Interactions of zebrafish peptide YYb with the neuropeptide Y-family receptors Y4, Y7, Y8a, and Y8b. Front Neurosci 7:29 Tao YX (2005) Molecular mechanisms of the neural melanocortin receptor dysfunction in severe early onset obesity. Mol Cell Endocrinol 239:1–14 Tao YX (2007) Functional characterization of novel melanocortin-3 receptor mutations identified from obese subjects. Biochim Biophys Acta 1772:1167–1174 Tao YX (2008) Constitutive activation of G protein-coupled receptors and diseases: insights into mechanism of activation and therapeutics. Pharmacol Ther 120:129–148 Tao YX (2009) Mutations in melanocortin-4 receptor and human obesity. Prog Mol Biol Transl Sci 88:173–204 Tao Y-X (2010) The melanocortin-4 receptor: physiology, pharmacology, and pathophysiology. Endocr Rev 31:506–543 Tao YX (2020) Molecular chaperones and G protein-coupled receptor maturation and pharmacology. Mol Cell Endocrinol 511:110862 Tao YX, Segaloff DL (2004) Functional characterization of melanocortin-3 receptor variants identify a loss-of-function mutation involving an amino acid critical for G protein-coupled receptor activation. J Clin Endocrinol Metab 89:3936–3942 Tao YX, Yuan ZH, Xie J (2013) G protein-coupled receptors as regulators of energy homeostasis. Prog Mol Biol Transl Sci 114:1–43 Tao M, Ji RL, Huang L, Fan SY, Liu T, Liu SJ, Tao YX (2020) Regulation of melanocortin-4 receptor pharmacology by two isoforms of melanocortin receptor accessory protein 2 in topmouth culter (Culter alburnus). Front Endocrinol 11:538 Tatemoto K (1982) Neuropeptide Y: complete amino acid sequence of the brain peptide. Proc Natl Acad Sci USA 79:5485–5489 Thomsen ARB, Plouffe B, Cahill TJ III, Shukla AK, Tarrasch JT, Dosey AM, Kahsai AW, Strachan RT, Pani B, Mahoney JP (2016) GPCR-G protein-β-arrestin super-complex mediates sustained G protein signaling. Cell 166:907–919 Vaisse C, Clement K, Guy-Grand B, Froguel P (1998) A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat Genet 20:113–114 van der Kraan M, Tatro JB, Entwistle ML, Brakkee JH, Burbach JP, Adan RA, Gispen WH (1999) Expression of melanocortin receptors and pro-opiomelanocortin in the rat spinal cord in relation to neurotrophic effects of melanocortins. Mol Brain Res 63:276–286 Volkoff H (2016) The neuroendocrine regulation of food intake in fish: a review of current knowledge. Front Neurosci 10:540 Volkoff H, Canosa LF, Unniappan S, Cerda-Reverter JM, Bernier NJ, Kelly SP, Peter RE (2005) Neuropeptides and the control of food intake in fish. Gen Comp Endocrinol 142:3–19 Wang F, Chen W, Lin H, Li WJ (2014) Cloning, expression, and ligand-binding characterization of two neuropeptide Y receptor subtypes in orange-spotted grouper, Epinephelus coioides. Fish Physiol Biochem 40:1693–1707 Wang T, Liang J, Xiang X, Chen X, Zhang B, Zhou N, Huang W, Yang J (2019) Pharmacological characterization, cellular localization and expression profile of NPY receptor subtypes Y2 and Y7 in large yellow croaker, Larimichthys crocea. Comp Biochem Physiol B 238:110347 Wei R, Yuan D, Zhou C, Wang T, Lin F, Chen H, Wu H, Xin Z, Yang S, Chen D, Wang Y, Liu J, Gao Y, Li Z (2013) Cloning, distribution and effects of fasting status of melanocortin 4 receptor (MC4R) in Schizothorax prenanti. Gene 532:100–107 Won ET, Borski RJ (2013) Endocrine regulation of compensatory growth in fish. Front Endocrinol 4:74 Yang H, Yang L (2016) Targeting cAMP/PKA pathway for glycemic control and type 2 diabetes therapy. J Mol Endocrinol 57:R93–R108 Yang LK, Zhang ZR, Wen HS, Tao YX (2019) Characterization of channel catfish (Ictalurus punctatus) melanocortin-3 receptor reveals a potential network in regulation of energy homeostasis. Gen Comp Endocrinol 277:90–103 Yang Z, Liang XF, Li GL, Tao YX (2020) Biased signaling in fish melanocortin-4 receptors (MC4Rs): Divergent pharmacology of four ligands on spotted scat (Scatophagus argus) and grass carp (Ctenopharyngodon idella) MC4Rs. Mol Cell Endocrinol 515:110929 Yeo GS, Farooqi IS, Aminian S, Halsall DJ, Stanhope RG, O’Rahilly S (1998) A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat Genet 20:111–112 Yi TL, Yang LK, Ruan GL, Yang DQ, Tao YX (2018) Melanocortin-4 receptor in swamp eel (Monopterus albus): Cloning, tissue distribution, and pharmacology. Gene 678:79–89 Zhang KQ, Hou ZS, Wen HS, Li Y, Qi X, Li WJ, Tao YX (2019) Melanocortin-4 receptor in spotted sea bass, Lateolabrax maculatus: cloning, tissue distribution, physiology, and pharmacology. Front Endocrinol 10:705 Zhang Y, Wen HS, Li Y, Lyu LK, Zhang ZX, Wang XJ, Li JS, Tao YX, Qi X (2020) Melanocortin-4 receptor regulation of reproductive function in black rockfish (Sebastes schlegelii). Gene 741:144541