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Characterization and expression analysis of two distinct neuropeptide Ya paralogues in Jian carp (Cyprinus carpio var. Jian)

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Abstract

Two distinct neuropeptide Ya paralogues (jlNPYa1 and jlNPYa2) were cloned and characterized in Jian carp (Cyprinus carpio var. Jian), with a highly conserved organization encoded by four exons and three introns. The cDNAs for jlNPYa1 and jlNPYa2 were 693 and 730 bp in size, respectively. jlNPYa1 and jlNPYa2 both encoded a 96-amino acid protein, which shared 97.9 % identity. Phylogenetic tree showed that it has two NPYa genes, called jlNPYa1 and jlNPYa2, that presumably resulted from the tetraploidization event in the carp lineage. Analysis of expression profiles of jlNPYa1 and jlNPYa2 showed that the two NPY genes had a broad tissue distribution but expressed primarily in the forebrain, hypothalamus, testis and liver. The expression pattern was different in juvenile and adult (female and male) Jian carp. In juvenile, the highest expression level of jlNPYa1 and jlNPYa2 was detected in the testis. In adult, it was detected in the forebrain. In female hypothalamus, the expression level of jlNPYa1 was significantly higher than that of jlNPYa2. However, the opposite was true in male hypothalamus. The differing distribution patterns of the two NPY genes suggested that jlNPYa1 and jlNPYa2 might play different roles in Jian carp.

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References

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brunet FG, Roest CH, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23:1808–1816

    Article  CAS  PubMed  Google Scholar 

  • Cerdá-Reverter JM, Anglade I, Martinez-Rodriguez G, Mazurais D, Munoz-Cueto JA, Carrillo M, Kah O, Zanuy S (2000) Characterization of neuropeptide Y expression in the brain of a perciform fish, the sea bass (Dicentrarchus labrax). J Chem Neuroanat 19:197–210

    Article  PubMed  Google Scholar 

  • Chambers KE, McDaniell R, Raincrow JD, Deshmukh M, Stadler PF, Chiu CH (2009) Hox cluster duplication in the basal teleost Hiodon alosoides (Osteoglossomorpha). Theory Biosci 128:109–120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 Physiol B 160:166–173

    Article  PubMed  Google Scholar 

  • Hsieh YS, Chen PN, Yu CH, Liao JM, Kuo DY (2013) The neuropeptide Y Y1 receptor knockdown modulates activator protein 1-involved feeding behavior in amphetamine-treated rats. Mol Brain 6:46

    Article  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957

    Article  PubMed  Google Scholar 

  • Kamijo M, Kojima K, Maruyama K, Konno N, Motohashi E, Ikegami T, Uchiyama M, Shioda S, Ando H, Matsuda K (2011) Neuropeptide Y in tiger puffer (Takifugu rubripes): distribution, cloning, characterization and mRNA expression responses to prandial condition. Zool Sci 28:882–890

    Article  CAS  PubMed  Google Scholar 

  • Kanatani A, Mashiko S, Murai N, Sugimoto N, Ito J, Fukuroda T, Fukami T, Morin N, MacNeil DJ, Van der Ploeg LH, Saga Y, Nishimura S, Ihara M (2000) Role of the Y1 receptor in the regulation of neuropeptide Y-mediated feeding: comparison of wild-type, Y1 receptor-deficient, and Y5 receptor-deficient mice. Endocrinology 141:1011–1016

    Article  CAS  PubMed  Google Scholar 

  • Kehoe AS, Volkoff H (2007) Cloning and characterization of neuropeptide Y (NPY) and cocaine and amphetamine regulated transcript (CART) in Atlantic cod (Gadus morhua). Comp Biochem Physiol A 146:451–461

    Article  Google Scholar 

  • Kenneth JL, Thomas DS (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−△△Ct method. Methods 25:402–408

    Article  Google Scholar 

  • Larhammar D, Bergqvist CA (2013) Ancient grandeur of the vertebrate neuropeptide Y system shown by the coelacanth Latimeria chalumnae. Front Neurosci 7:27

    Article  PubMed Central  PubMed  Google Scholar 

  • Larsson TA, Olsson F, Sundstrom G, Lundin LG, Brenner S, Venkatesh B, Larhammar D (2008) Early vertebrate chromosome duplications and the evolution of the neuropeptide Y receptor gene regions. BMC Evol Biol 8:184

    Article  PubMed Central  PubMed  Google Scholar 

  • Larsson TA, Tay BH, Sundström G, Fredriksson R, Brenner S, Larhammar D, Venkatesh B (2009) Neuropeptide Y-family peptides and receptors in the elephant shark, Callorhinchus milii confirm gene duplications before the gnathostome radiation. Genomics 93:254–260

    Article  CAS  PubMed  Google Scholar 

  • MacDonald E, Volkoff H (2009) Neuropeptide Y (NPY), cocaine and amphetamine regulated transcript (CART) and cholecystokinin (CCK) in winter skate (Raja ocellata): cDNA cloning, tissue distribution and mRNA expression responses to fasting. Gen Comp Endocrinol 161:252–261

    Article  CAS  PubMed  Google Scholar 

  • Mazumdar M, Sakharkar AJ, Singru PS, Subhedar N (2007) Reproduction phase-related variations in neuropeptide Y immunoreactivity in the olfactory system, forebrain, and pituitary of the female catfish, Clarias batrachus (Linn). J Comp Neurol 504:450–469

    Article  CAS  PubMed  Google Scholar 

  • Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945

    Article  CAS  PubMed  Google Scholar 

  • Murashita K, Kurokawa T, Ebbesson LO, Stefansson SO, Rønnestad I (2009) Characterization, tissue distribution, and regulation of agouti-related protein (AgRP), cocaine- and amphetamine-regulated transcript (CART) and neuropeptide Y (NPY) in Atlantic salmon (Salmo salar). Gen Comp Endocrinol 162:160–171

    Article  CAS  PubMed  Google Scholar 

  • Narnaware YK, Peyon PP, Lin X, Peter RE (2000) Regulation of food intake by neuropeptide Y in goldfish. Am J Physiol Regul Intergr Comp Physiol 279:R1025–R1034

    CAS  Google Scholar 

  • Nguyen AD, Herzog H, Sainsbury A (2011) Neuropeptide Y and peptide YY: important regulators of energy metabolism. Curr Opin Endocrinol Diabetes Obes 18:56–60

    Article  CAS  PubMed  Google Scholar 

  • Polidori C, Ciccocioppo R, Regoli D, Massi M (2000) Neuropeptide Y receptor(s) mediating feeding in the rat: characterization with antagonists. Peptides 21:29–35

    Article  CAS  PubMed  Google Scholar 

  • Sakharkar AJ, Singru PS, Sarkar K, Subhedar NK (2005) Neuropeptide Y in the forebrain of the adult male cichlid fish Oreochromis mossambicus: distribution, effects of castration and testosterone replacement. J Comp Neurol 489:148–165

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Nishida M (2010) Teleost fish with specific genome duplication as unique models of vertebrate evolution. Environ Biol Fish 88:169–188

    Article  Google Scholar 

  • Semon M, Wolfe KH (2007) Reciprocal gene loss between Tetraodon and zebrafish after whole genome duplication in their ancestor. Trends Genet 23:108–112

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Söderberg C, Wraith A, Ringvall M, Yan YL, Postlethwait JH, Brodin L, Larhammar D (2000) Zebrafish genes for neuropeptide Y and peptide YY reveal origin by chromosome duplication from an ancestral gene linked to the homeobox cluster. J Neurochem 75:908–918

    Article  PubMed  Google Scholar 

  • Sundström G, Larsson TA, Brenner S, Venkatesh B, Larhammar D (2008) Evolution of the neuropeptide Y family: new genes by chromosome duplications in early vertebrates and in teleost fishes. Gen Comp Endocrinol 155:705–716

    Article  PubMed  Google Scholar 

  • Tang YK, Yu JH, Xu P, Li JL, Li HX, Ren HT (2012) Identification of housekeeping genes suitable for gene expression analysis in Jian carp (Cyprinus carpio var Jian). Fish Shellfish Immunol 33:775–779

    Article  CAS  PubMed  Google Scholar 

  • Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y—a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660

    Article  CAS  PubMed  Google Scholar 

  • Taylor JS, Braasch I, Frickey T, Meyer A, Van de PY (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13:382–390

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Volkoff H (2006) The role of neuropeptide Y, orexins, cocaine and amphetamine-related transcript, cholecystokinin, amylin and leptin in the regulation of feeding in fish. Comp Biochem Physiol A 144:325–331

    Article  Google Scholar 

  • Volkoff H, Canosa LF, Unniappan S, Cerdá-Reverter JM, Bernier NJ, Kelly SP, Peter RE (2005) Neuropeptides and the control of food intake in fish. Gen Comp Endocrinol 142:3–19

    Article  CAS  PubMed  Google Scholar 

  • Wang JT, Li JT, Zhang XT, Sun XW (2012) Transcriptome analysis reveals the time of the fourth round of genome duplication in common carp (Cyprinus carpio). BMC Genom 13:96

    Article  CAS  Google Scholar 

  • Wheway J, Herzog H, Mackay F (2007) NPY and receptors in immune and inflammatory diseases. Curr Top Med Chem 7:1743–1752

    Article  CAS  PubMed  Google Scholar 

  • Wolfe KH (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2:333–341

    Article  CAS  PubMed  Google Scholar 

  • Yokobori E, Azuma M, Nishiguchi R, Kang KS, Kamijo M, Uchiyama M, Matsuda K (2012) Neuropeptide Y stimulates food intake in the zebrafish, Danio rerio. J Neuroendocrinol 24:766–773

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Yagi M, Herzog H (2012) The role of NPY and ghrelin in anorexia nervosa. Curr Pharm Des 18:4766–4778

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Liang XF, Yuan XC, Li J, He Y, Fang L, Guo XZ, Liu LW, Li B, Shen D (2013) Neuropeptide Y stimulates food intake and regulates metabolism in grass carp. Ctenopharyngodon idellus Aquaculture 380–383:52–61

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by National “863” Program of China (2011AA100401), National Technology System for Conventional Freshwater Fishery Industry (CARS-46) and Special Research Fund at Central Nonprofit Research Institutes (2013JBFM03).

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Authors and Affiliations

  1. Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, China

    Yongkai Tang, Hongxia Li, Jianlin Li, Fan Yu & Juhua Yu

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  1. Yongkai Tang
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  2. Hongxia Li
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  3. Jianlin Li
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  4. Fan Yu
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  5. Juhua Yu
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Correspondence to Juhua Yu.

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Tang, Y., Li, H., Li, J. et al. Characterization and expression analysis of two distinct neuropeptide Ya paralogues in Jian carp (Cyprinus carpio var. Jian). Fish Physiol Biochem 40, 1709–1719 (2014). https://doi.org/10.1007/s10695-014-9961-4

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