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Abstract:

The proopiomelanocortin gene (POMC) encodes several bioactive peptides, including adrenocorticotropin hormone, α-, β-, and γ-melanocyte-stimulating hormone, and the opioid peptide β-endorphin, which play key roles in vertebrate physiology. In the human, mouse, and chicken genomes, there is only one POMC gene. By searching public genome projects, we have found that Tetraodon (Tetraodon nigroviridis), Fugu (Takifugu rubripes), and zebrafish (Danio rerio) possess two POMC genes, which we called POMCα and POMCβ, and we present phylogenetic and mapping evidence that these paralogue genes originated in the whole-genome duplication specific to the teleost lineage over 300 MYA. In addition, we present evidence for two types of subfunction partitioning between the paralogues. First, in situ hybridization experiments indicate that the expression domains of the ancestral POMC gene have been subfunctionalized in Tetraodon, with POMCα expressed in the nucleus lateralis tuberis of the hypothalamus, as well as in the rostral pars distalis and pars intermedia (PI) of the pituitary, whereas POMCβ is expressed in the preoptic area of the brain and weakly in the pituitary PI. Second, POMCβ genes have a β-endorphin segment that lacks the consensus opioid signal and seems to be under neutral evolution in tetraodontids, whereas POMCα genes possess well-conserved peptide regions. Thus, POMC paralogues have experienced subfunctionalization of both expression and peptide domains during teleost evolution. The study of regulatory regions of fish POMC genes might shed light on the mechanisms of enhancer partitioning between duplicate genes, as well as the roles of POMC-derived peptides in fish physiology.

Registro:

Documento: Artículo
Título:Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes
Autor:De Souza, F.S.J.; Bumaschny, V.F.; Low, M.J.; Rubinstein, M.
Filiación:Instituto de Investigaciones en Ingeniería Genética Y Biología Molecular, CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Fisiología, Biología Molecular Y Celular, FCEyN, Universidad de Buenos Aires, Buenos Aires, Argentina
Vollum Institute, Oregon Health and Science University, Valdivia, Chile
Department of Behavioral Neuroscience, Oregon Health and Science University, Valdivia, Chile
Center for the Study of Weight Regulation and Associated Disorders, Oregon Health and Science University, Valdivia, Chile
Centro de Estudios Científicos, Valdivia, Chile
Palabras clave:β-endorphin; Evolution; POMC; Subfunctionalization; Teleosts; Tetraodon; opiate; proopiomelanocortin; article; gene duplication; gene mapping; hypophysis; hypothalamus nucleus; in situ hybridization; molecular evolution; nonhuman; nucleotide sequence; phylogeny; preoptic area; protein domain; protein expression; protein function; signal transduction; teleost; Amino Acid Sequence; Animals; Evolution, Molecular; Fishes; Gene Duplication; Molecular Sequence Data; Phylogeny; Pro-Opiomelanocortin; Sequence Alignment; Tetraodontiformes; Zebrafish; Danio rerio; Takifugu; Takifugu rubripes; Teleostei; Tetraodon; Tetraodon nigroviridis; Tetraodontidae; Vertebrata
Año:2005
Volumen:22
Número:12
Página de inicio:2417
Página de fin:2427
DOI: http://dx.doi.org/10.1093/molbev/msi236
Título revista:Molecular Biology and Evolution
Título revista abreviado:Mol. Biol. Evol.
ISSN:07374038
CODEN:MBEVE
CAS:opiate, 53663-61-9, 8002-76-4, 8008-60-4; proopiomelanocortin, 66796-54-1; Pro-Opiomelanocortin, 66796-54-1
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_07374038_v22_n12_p2417_DeSouza.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_07374038_v22_n12_p2417_DeSouza

Referencias:

  • Altschmied, J., Delfgaauw, J., Wilde, B., Duschl, J., Bouneau, L., Volff, J.N., Schartl, M., Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish (2002) Genetics, 161, pp. 259-267
  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool (1990) J. Mol. Biol., 215, pp. 403-410
  • Amano, M., Takahashi, A., Yamanome, T., Oka, Y., Amyia, N., Kawauchi, H., Yamamori, K., Immunocytochemical localization and ontogenic development of α-melanocyte stimulating hormone (α-MSH) in the brain of a pleuronectiform fish, barfin flounder (2005) Cell Tissue Res., 320, pp. 127-134
  • Aparicio, S., Chapman, J., Stupka, E., Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes (2002) Science, 297, pp. 1301-1310
  • Benton, M.J., (2000) Vertebrate Palaeontogy. 2nd Edition, , Blackwell Science, Oxford
  • Christoffels, A., Koh, E.G., Chia, J.M., Brenner, S., Aparicio, S., Venkatesh, B., Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes (2004) Mol. Biol. Evol., 21, pp. 1146-1151
  • David, L., Blum, S., Feldman, M.W., Lavi, U., Hillel, J., Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci (2003) Mol. Biol. Evol., 20, pp. 1425-1434
  • De Souza, F.S., Santangelo, A.M., Bumaschny, V., Avale, M.E., Smart, J.L., Low, M.J., Rubinstein, M., Identification of neuronal enhancers of the proopiomelanocortin gene by transgenic mouse analysis and phylogenetic footprinting (2005) Mol. Cell. Biol., 25, pp. 3076-3086
  • Dores, R.M., Lecaude, S., Trends in the evolution of the proopiomelanocortin gene (2005) Gen. Comp. Endocrinol., 142, pp. 81-93
  • Dores, R.M., Sollars, C., Danielson, P., Lee, J., Alrubaian, J., Joss, J.M., Cloning of a proopiomelanocortin cDNA from the pituitary of the Australian lungfish, Neoceratodus forsteri: Analyzing trends in the organization of this prohormone precursor (1999) Gen. Comp. Endocrinol., 116, pp. 433-444
  • Felsenstein, J., (2004) PHYLIP (Phylogeny Inference Package). Version 3.6, , Distributed by the author, Department of Genome Sciences, University of Washington, Seattle
  • Ficele, G., Heinig, J.A., Kawauchi, H., Youson, J.H., Keeley, F.W., Wright, G.M., Spatial and temporal distribution of proopiomelanotropin and proopiocortin mRNA during the life cycle of the sea lamprey: A qualitative and quantitative in situ hybridization study (1998) Gen. Comp. Endocrinol., 110, pp. 212-225
  • Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L., Postlethwait, J.H., Preservation of duplicate genes by complementary, degenerative mutations (1999) Genetics, 151, pp. 1531-1545
  • González-Nuñez, V., González-Sarmiento, R., Rodríguez, R.E., Identification of two proopiomelanocortin genes in zebrafish (Danio rerio) (2003) Brain Res. Mol. Brain Res., 120, pp. 1-8
  • Hadley, M.E., Haskell-Luevano, C., The proopiomelanocortin system (1999) Ann. N. Y. Acad. Sci., 885, pp. 1-21
  • Hansen, I.A., To, T.T., Wortmann, S., Burmester, T., Winkler, C., Meyer, S.R., Neuner, C., Allolio, B., The pro-opiomelanocortin gene of the zebrafish (Danio rerio) (2003) Biochem. Biophys. Res. Commun., 303, pp. 1121-1128
  • Herzog, W., Zeng, X., Lele, Z., Sonntag, C., Ting, J.W., Chang, C.Y., Hammerschmidt, M., Adenohypophysis formation in the zebrafish and its dependence on sonic hedgehog (2003) Dev. Biol., 254, pp. 36-49
  • Hoegg, S., Brinkmann, H., Taylor, J.S., Meyer, A., Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish (2004) J. Mol. Evol., 59, pp. 190-203
  • Huang, F.D., Matthies, H.J., Speese, S.D., Smith, M.A., Broadie, K., Rolling blackout, a newly identified PIP2-DAG pathway lipase required for Drosophila phototransduction (2004) Nat. Neurosci., 7, pp. 1070-1078
  • Hurst, L.D., The Ka/Ks ratio: Diagnosing the form of sequence evolution (2002) Trends Genet., 18, p. 486
  • Inoue, J.G., Miya, M., Tsukamoto, K., Nishida, M., Basal actinopterygian relationships: A mitogenomic perspective on the phylogeny of the "ancient fish" (2003) Mol. Phylogenet. Evol., 26, pp. 110-120
  • Mitogenomic evidence for the monophyly of elopomorph fishes (Teleostei) and the evolutionary origin of the leptocephalus larva (2004) Mol. Phylogenet. Evol., 32, pp. 274-286
  • Jaillon, O., Aury, J.M., Brunet, F., Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype (2004) Nature, 431, pp. 946-957
  • Jones, D.T., Taylor, W.R., Thornton, J.M., The rapid generation of mutation data matrices from protein sequences (1992) CABIOS, 8, pp. 275-282
  • Kikugawa, K., Katoh, K., Kuraku, S., Sakurai, H., Ishida, O., Iwabe, N., Miyata, T., Basal jawed vertebrate phylogeny inferred from multiple nuclear DNA-coded genes (2004) BMC Biol., 2, p. 3
  • Klovins, J., Haitina, T., Fridmanis, D., Kilianova, Z., Kapa, I., Fredriksson, R., Gallo-Payet, N., Schiöth, H.B., The melanocortin system in Fugu: Determination of POMC/AGRP/MCR gene repertoire and synteny, as well as pharmacology and anatomical distribution of the MCRs (2004) Mol. Biol. Evol., 21, pp. 563-579
  • Kumar, S., Hedges, S.B., A molecular timescale for vertebrate evolution (1998) Nature, 392, pp. 917-920
  • Liu, N.A., Huang, H., Yang, Z., Herzog, W., Hammerschmidt, M., Lin, S., Melmed, S., Pituitary corticotroph ontogeny and regulation in transgenic zebrafish (2003) Mol. Endocrinol., 17, pp. 959-966
  • Liu, R.Z., Sun, Q., Thisse, C., Thisse, B., Wright, J.M., Denovan-Wright, E.M., The cellular retinol-binding protein genes are duplicated and differentially transcribed in the developing and adult zebrafish (Danio rerio) (2005) Mol. Biol. Evol., 22, pp. 469-477
  • Low, M.J., Somatostatin (2003) Encyclopedia of Hormones, pp. 379-388. , H. L. Henry and A. W. Norman, eds. Elsevier Science, San Diego, Calif
  • Ludwig, A., Belfiore, N.M., Pitra, C., Svirsky, V., Jenneckens, I., Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus) (2001) Genetics, 158, pp. 1203-1215
  • McClintock, J.M., Kheirbek, M.A., Prince, V.E., Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention (2002) Development, 129, pp. 2339-2354
  • Metz, J.R., Huising, M.O., Meek, J., Taverne-Thiele, A.J., Wendelaar-Bonga, S.E., Flik, G., Localization, expression and control of adrenocorticotropic hormone in the nucleus preopticus and pituitary gland of the common carp (Cyprinus carpio L.) (2004) J. Endocrinol., 182, pp. 23-31
  • Palti, Y., Gahr, S.A., Hansen, J.D., Rexroad III, C.E., Characterization of a new BAC library for rainbow trout: Evidence for multi-locus duplication (2004) Anim. Genet., 35, pp. 130-133
  • Pandolfi, M., Canepa, M.M., Ravaglia, M.A., Maggese, M.C., Paz, D.A., Vissio, P.G., Melanin-concentrating hormone system in the brain and skin of the cichlid fish Cichlasoma dimerus: Anatomical localization, ontogeny and distribution in comparison to α-melanocyte-stimulating hormone-expressing cells (2003) Cell Tissue Res., 311, pp. 61-69
  • Postlethwait, J., Amores, A., Cresko, W., Singer, A., Yan, Y.L., Subfunction partitioning, the teleost radiation and the annotation of the human genome (2004) Trends Genet., 20, pp. 481-490
  • Reinscheid, R.K., Nothacker, H.P., Bourson, A., Ardati, A., Henningsen, R.A., Bunzow, J.R., Grandy, D.K., Civelli, O., Orphanin FQ: A neuropeptide that activates an opioidlike G protein-coupled receptor (1995) Science, 270, pp. 792-794
  • Rozas, J., Rozas, R., DnaSP version 3: An integrated program for molecular population genetics and molecular evolution analysis (1999) Bioinformatics, 15, pp. 174-175
  • Rubinstein, M., Mortrud, M., Liu, B., Low, M.J., Rat and mouse proopiomelanocortin gene sequences target tissue-specific expression to the pituitary gland but not to the hypothalamus of transgenic mice (1993) Neuroendocrinology, 58, pp. 373-380
  • Salbert, G., Chauveau, I., Bonnec, G., Valotaire, Y., Jego, P., One of the two trout proopiomelanocortin messenger RNAs potentially encodes new peptides (1992) Mol. Endocrinol., 6, pp. 1605-1613
  • Takahashi, A., Amano, M., Itoh, T., Yasuda, A., Yamanome, T., Amemyia, Y., Sasaki, T., Kawauchi, H., Nucleotide sequence and expression of three subtypes of proopiomelanocortion RNA in barfin flounder (2005) Gen. Comp. Endocrinol., 141, pp. 291-303
  • Takahashi, A., Amemiya, Y., Nozaki, M., Sower, S.A., Kawauchi, H., Evolutionary significance of proopiomelanocortin in agnatha and chondrichthyes (2001) Comp. Biochem. Physiol. B Biochem. Mol. Biol., 129, pp. 283-289
  • Taylor, J.S., Braasch, I., Frickey, T., Meyer, A., Van De Peer, Y., Genome duplication, a trait shared by 22,000 species of ray-finned fish (2003) Genome Res., 13, pp. 382-390
  • Taylor, J.S., Van De Peer, Y., Braasch, I., Meyer, A., Comparative genomics provides evidence for an ancient genome duplication event in fish (2001) Philos. Trans. R. Soc. Lond. B Biol. Sci., 356, pp. 1661-1679
  • Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice (1994) Nucleic Acids Res., 22, pp. 4673-4680
  • Tuinhof, R., Ubink, R., Tanaka, S., Atzori, C., Van Strien, F.J., Roubos, E.W., Distribution of pro-opiomelanocortin and its peptide end products in the brain and hypophysis of the aquatic toad, Xenopus laevis (1998) Cell Tissue Res., 292, pp. 251-265
  • Vallarino, M., Tranchand Bunel, D., Vaudry, H., α-melanocyte-stimulating hormone (α-MSH) in the brain of the African lungfish, Protopterus annectens: Immunohistochemical localization and biochemical characterization (1992) J. Comp. Neurol., 322, pp. 266-274
  • Vandepoele, K., De Vos, W., Taylor, J.S., Meyer, A., Van De Peer, Y., Major events in the genome evolution of vertebrates: Paranome age and size differ considerably between ray-finned fishes and land vertebrates (2004) Proc. Natl. Acad. Sci., 101, pp. 1638-1643. , USA
  • Volff, J.N., Genome evolution and biodiversity in teleost fish (2005) Heredity, 94, pp. 280-294
  • Volkoff, H., Canosa, L.F., Unniappan, S., Cerda-Reverter, J.M., Bernier, N.J., Kelly, S.P., Peter, R.E., Neuropeptides and the control of food intake in fish (2005) Gen. Comp. Endocrinol., 142, pp. 3-19
  • Waldhoer, M., Bartlett, S.E., Whistler, J.L., Opioid receptors (2004) Annu. Rev. Biochem., 73, pp. 953-990
  • Woods, I.G., Kelly, P.D., Chu, F., Ngo-Hazelett, P., Yan, Y.L., Huang, H., Postlethwait, J.H., Talbot, W.S., A comparative map of the zebrafish genome (2000) Genome Res., 10, pp. 1903-1910

Citas:

---------- APA ----------
De Souza, F.S.J., Bumaschny, V.F., Low, M.J. & Rubinstein, M. (2005) . Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes. Molecular Biology and Evolution, 22(12), 2417-2427.
http://dx.doi.org/10.1093/molbev/msi236
---------- CHICAGO ----------
De Souza, F.S.J., Bumaschny, V.F., Low, M.J., Rubinstein, M. "Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes" . Molecular Biology and Evolution 22, no. 12 (2005) : 2417-2427.
http://dx.doi.org/10.1093/molbev/msi236
---------- MLA ----------
De Souza, F.S.J., Bumaschny, V.F., Low, M.J., Rubinstein, M. "Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes" . Molecular Biology and Evolution, vol. 22, no. 12, 2005, pp. 2417-2427.
http://dx.doi.org/10.1093/molbev/msi236
---------- VANCOUVER ----------
De Souza, F.S.J., Bumaschny, V.F., Low, M.J., Rubinstein, M. Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes. Mol. Biol. Evol. 2005;22(12):2417-2427.
http://dx.doi.org/10.1093/molbev/msi236