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Gaillard, A.-L.; Tay, B.-H.; Sirkin, D.I.P.; Lafont, A.-G.; De Flori, C.; Vissio, P.G.; Mazan, S.; Dufour, S.; Venkatesh, B.; Tostivint, H. "Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives" (2018) Frontiers in Neuroscience. 12(SEP)
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Abstract:

The neuropeptide gonadotropin-releasing hormone (GnRH) plays an important role in the control of reproductive functions. Vertebrates possess multiple GnRH forms that are classified into three main groups, namely GnRH1, GnRH2, and GnRH3. In order to gain more insights into the GnRH gene family in vertebrates, we sought to identify which paralogs of this family are present in cartilaginous fish. For this purpose, we searched the genomes and/or transcriptomes of three representative species of this group, the small-spotted catshark, Scyliorhinus canicula, the whale shark, Rhincodon typus and the elephant shark Callorhinchus milii. In each species, we report the identification of three GnRH genes. In catshark and whale shark, phylogenetic and synteny analysis showed that these three genes correspond to GnRH1, GnRH2, and GnRH3. In both species, GnRH1 was found to encode a novel form of GnRH whose primary structure was determined as follows: QHWSFDLRPG. In elephant shark, the three genes correspond to GnRH1a and GnRH1b, two copies of the GnRH1 gene, plus GnRH2. 3D structure prediction of the chondrichthyan GnRH-associated peptides (GAPs) revealed that catshark GAP1, GAP2, and elephant shark GAP2 peptides exhibit a helix-loop-helix (HLH) structure. This structure observed for many osteichthyan GAP1 and GAP2, may convey GAP biological activity. This HLH structure could not be observed for elephant shark GAP1a and GAP1b. As for all other GAP3 described so far, no typical 3D HLH structure was observed for catshark nor whale shark GAP3. RT-PCR analysis revealed that GnRH1, GnRH2, and GnRH3 genes are differentially expressed in the catshark brain. GnRH1 mRNA appeared predominant in the diencephalon while GnRH2 and GnRH3 mRNAs seemed to be most abundant in the mesencephalon and telencephalon, respectively. Taken together, our results show that the GnRH gene repertoire of the vertebrate ancestor was entirely conserved in the chondrichthyan lineage but that the GnRH3 gene was probably lost in holocephali. They also suggest that the three GnRH neuronal systems previously described in the brain of bony vertebrates are also present in cartilaginous fish. © 2018 Gaillard, Tay, Pérez Sirkin, Lafont, De Flori, Vissio, Mazan, Dufour, Venkatesh and Tostivint.

Registro:

Documento: Artículo
Título:Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives
Autor:Gaillard, A.-L.; Tay, B.-H.; Sirkin, D.I.P.; Lafont, A.-G.; De Flori, C.; Vissio, P.G.; Mazan, S.; Dufour, S.; Venkatesh, B.; Tostivint, H.
Filiación:Evolution des Régulations Endocriniennes UMR 7221 CNRS, Muséum National d'Histoire Naturelle, Paris, France
Institute of Molecular and Cell Biology, A-STAR, Biopolis, Singapore
Laboratorio de Neuroendocrinología del Crecimiento y la Reproducción, Facultad de Ciencias Exactas y Naturales, DBBE/IBBEA-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Biologie des Organismes et Ecosystèmes Aquatiques, CNRS, Muséum National d'Histoire Naturelle, Sorbonne Université, Paris, France
Biologie Intégrative des Organismes Marins, UMR 7232 CNRS, Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, France
Palabras clave:Cartilaginous fish; Elasmobranchii; Evolution; Gonadotropin-releasing hormone; Holocephali; Multigenic family; Neuropeptides; Vertebrates; gonadorelin; gonadorelin associated peptide; helix loop helix protein; messenger RNA; protein GAP1a; protein GAP1b; protein GAP3; unclassified drug; animal tissue; Article; Callorhinchus milii; cartilaginous fish; controlled study; diencephalon; enzyme activity; female; gene; gene dosage; gene expression; gene identification; gene structure; genetic trait; genome; GnRH gene; GnRH1 gene; GnRH1a gene; GnRH1b gene; GnRH2 gene; GnRH3 gene; Holocephali; male; mesencephalon; nerve cell; nonhuman; nucleotide sequence; phylogeny; prediction; protein structure; reverse transcription polymerase chain reaction; Rhincodon typus; Scyliorhinus canicula; shark; synteny; telencephalon; transcriptomics
Año:2018
Volumen:12
Número:SEP
DOI: http://dx.doi.org/10.3389/fnins.2018.00607
Título revista:Frontiers in Neuroscience
Título revista abreviado:Front. Neurosci.
ISSN:16624548
CAS:gonadorelin, 33515-09-2, 9034-40-6; gonadorelin associated peptide, 124375-77-5
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_16624548_v12_nSEP_p_Gaillard

Referencias:

  • Abascal, F., Zardoya, R., Posada, D., ProtTest: selection of best-fit models of protein evolution (2005) Bioinformatics, 21, pp. 2104-2105
  • 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
  • Ashihara, M., Suzuki, M., Kubokawa, K., Yoshiura, Y., Kobayashi, M., Urano, A., Two differing precursor genes for the salmon-type gonadotropin-releasing hormone exist in salmonids (1995) J. Mol. Endocrinol, 15, pp. 1-9
  • Awruch, C.A., Reproductive endocrinology in chondrichthyans: the present and the future (2013) Gen. Comp. Endocrinol, 192, pp. 60-70
  • Beaudoing, E., Freier, S., Wyatt, J.R., Claverie, J.M., Gautheret, D., Patterns of variant polyadenylation signal usage in human genes (2000) Genome Res, 10, pp. 1001-1010
  • Boetzer, M., Henkel, C.V., Jansen, H.J., Butler, D., Pirovano, W., Scaffolding pre-assembled contigs using SSPACE (2011) Bioinformatics, 27, pp. 578-579
  • Calvin, J.L., Slater, C.H., Bolduc, T.G., Laudano, A.P., Sower, S.A., Multiple molecular forms of gonadotropin-releasing hormone in the brain of an elasmobranch: evidence for IR-lamprey GnRH (1992) Peptides, 14, pp. 725-729
  • Clarke, I.J., Cummins, J.T., Karsch, F.J., Seeburg, P.H., Nikolics, K., GnRH-associated peptide (GAP) is cosecreted with GnRH into the hypophyseal portal blood of ovariectomized sheep (1987) Biochem. Biophys. Res. Commun, 143, pp. 665-671
  • Coolen, M., Menuet, A., Chassoux, D., Compagnucci, C., Henry, S., Lévèque, L., The dogfish Scyliorhinus canicula: a reference in jawed vertebrates (2008) Cold Spring Harb. Protoc, 2008
  • D'Antonio, M., Vallarino, M., Lovejoy, D.A., Vandesande, F., King, J.A., Pierantoni, R., Nature and distribution of gonadotropin-releasing hormone (GnRH) in the brain, and GnRH and GnRH binding activity in the serum of the spotted dogfish Scyliorhinus canicula (1995) Gen. Comp. Endocrinol, 98, pp. 35-49
  • Decatur, W.A., Hall, J.A., Smith, J.J., Li, W., Sower, S.A., Insight from the lamprey genome: glimpsing early vertebrate development via neuroendocrine-associated genes and shared synteny of gonadotropin-releasing hormone (GnRH) (2013) Gen. Comp. Endocrinol, 192, pp. 237-245
  • Dubois, E.A., Zandbergen, M.A., Peute, J., Goos, H.J., Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates (2002) Brain Res. Bull, 57, pp. 413-418
  • Fernald, R.D., White, R.B., Gonadotropin-releasing hormone genes: phylogeny, structure, and functions (1999) Front. Neuroendocrinol, 20, pp. 224-240
  • Gout, J.F., Kahn, D., Duret, L., The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution (2010) PLoS Genet, 6
  • Gouy, M., Guindon, S., Gascuel, O., Seaview version 4, a multiplatform graphical user interface for sequence alignment and phylogenetic tree building (2010) Mol. Biol. Evol, 27, pp. 221-224
  • Guindon, S., Gascuel, O., A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood (2003) Syst. Biol, 52, pp. 696-704
  • Gwee, P.C., Tay, B.H., Brenner, S., Venkatesh, B., Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: origin of the vertebrate neurohypophysial hormone genes (2009) BMC Evol. Biol, 9, p. 47
  • Kah, O., Lethimonier, C., Somoza, G., Guilgur, L.G., Vaillant, C., Lareyre, J.J., GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective (2007) Gen. Comp. Endocrinol, 153, pp. 346-364
  • Kavanaugh, S.I., Nozaki, M., Sower, S.A., Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey (2008) Endocrinology, 149, pp. 3860-3869
  • Kim, D.K., Cho, E.B., Moon, M.J., Park, S., Hwang, J.I., Kah, O., Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes (2011) Gen. Comp. Endocrinol, 170, pp. 68-78
  • Lien, S., Koop, B.F., Sandve, S.R., Miller, J.R., Kent, M.P., Nome, T., The Atlantic salmon genome provides insights into rediploidization (2016) Nature, 533, pp. 200-205
  • Lovejoy, D.A., Fischer, W.H., Ngamvongchon, S., Craig, A.G., Nahorniak, C.S., Peter, R.E., Distinct sequence of gonadotropin-releasing hormone (GnRH) in dogfish brain provides insight into GnRH evolution (1992) Proc. Natl. Acad. Sci. U.S.A, 89, pp. 6373-6377
  • Lovejoy, D.A., King, J.A., Sherwood, N.M., Peter, R.E., Identification of gonadotropin-releasing hormone and associated binding substances in the blood serum of a holocephalan (Hydrolagus colliei) (1993) Peptides, 14, pp. 1237-1243
  • Lovejoy, D.A., Michalec, O.M., Hogg, D.W., Wosnick, D.I., Role of elasmobranchs and holocephalans in understanding peptide evolution in the vertebrates: lessons learned from gonadotropin releasing hormone (GnRH) and corticotropin releasing factor (CRF) phylogenies (2017) Gen. Comp. Endocrinol, 264, pp. 78-83
  • Lovejoy, D.A., Sherwood, N.M., Fischer, W.H., Jackson, B.C., Rivier, J.E., Lee, T., Primary structure of gonadotropin-releasing hormone from the brain of a holocephalan (ratfish: Hydrolagus colliei) (1991) Gen. Comp. Endocrinol, 82, pp. 152-161
  • Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler (2012) Gigascience, 1, p. 18
  • Masini, M.A., Prato, P., Vacchi, M., Uva, B.M., GnRH immunodetection in the brain of the holocephalan fish Chimaera monstrosa L.: correlation to oocyte maturation (2008) Gen. Comp. Endocrinol, 156, pp. 559-563
  • Millar, R.P., GnRH II and type II GnRH receptors (2003) Trends Endocrinol. Metab, 14, pp. 35-43
  • Muffato, M., Louis, A., Poisnel, C.E., Roest Crollius, H., Genomicus: a database and a browser to study gene synteny in modern and ancestral genomes (2010) Bioinformatics, 26, pp. 1119-1121
  • Nelson, J.S., (2006) Fishes of the World, , 4th Edn Hoboken, NJ: Wiley
  • Nielsen, H., Predicting secretory proteins with signalP (2017) Methods Mol. Biol, 1611, pp. 59-73
  • Nikolics, K., Mason, A.J., Szönyi, É., Ramachandran, J., Seeburg, P.H., A prolactin-inhibiting factor within the precursor for human gonadotropin-releasing hormone (1985) Nature, 316, pp. 511-517
  • Nock, T.G., Chand, D., Lovejoy, D.A., Identification of members of the gonadotropin-releasing hormone (GnRH), corticotropin-releasing factor (CRF) families in the genome of the holocephalan, Callorhinchus milii (elephant shark) (2011) Gen. Comp. Endocrinol, 171, pp. 237-244
  • Okubo, K., Nagahama, Y., Structural and functional evolution of gonadotropin-releasing hormone in vertebrates (2008) Acta Physiol, 193, pp. 3-15
  • Pérez Sirkin, D.I., Lafont, A.G., Kamech, N., Somoza, G.M., Vissio, P.G., Dufour, S., Conservation of three-dimensional helix-loop-helix structure through the vertebrate lineage reopens the cold case of gonadotropin-releasing hormone-associated peptide (2017) Front. Endocrinol, 8, p. 207
  • Powell, R.C., Millar, R.P., King, J.A., Diverse molecular forms of gonadotropin-releasing hormone in an elasmobranch and a teleost fish (1986) Gen. Comp. Endocrinol, 63, pp. 77-85
  • Quan, F.B., Kenigfest, N.B., Mazan, S., Tostivint, H., Molecular cloning of the cDNAs encoding three somatostatin variants in the dogfish (Scylorhinus canicula) (2013) Gen. Comp. Endocrinol, 180, pp. 1-6
  • Read, T.D., Petit, R.A., III, Joseph, S.J., Alam, M.T., Weil, M.R., Ahmad, M., Draft sequencing and assembly of the genome of the world's largest fish, the whale shark: Rhincodon typus Smith 1828 (2017) BMC Genomics, 18, p. 532
  • Roch, G.J., Busby, E.R., Sherwood, N.M., GnRH receptors and peptides: skating backward (2014) Gen. Comp. Endocrinol, 209, pp. 118-134
  • Roch, G.J., Tello, J.A., Sherwood, N.M., At the transition from invertebrates to vertebrates, a novel GnRH-like peptide emerges in amphioxus (2014) Mol. Biol. Evol, 31, pp. 765-778
  • Session, A.M., Uno, Y., Kwon, T., Chapman, J.A., Toyoda, A., Takahashi, S., Genome evolution in the allotetraploid frog Xenopus laevis (2016) Nature, 538, pp. 336-343
  • Smith, J.J., Kuraku, S., Holt, C., Sauka-Spengler, T., Jiang, N., Campbell, M.S., Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution (2013) Nat. Genet, 45, pp. 415-421
  • Stingo, V., Du Buit, M.-H., Odierna, G., Genome size of some selachian fishes (1980) Boll. Zool, 47, pp. 129-137
  • Tostivint, H., Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations (2011) Gen. Comp. Endocrinol, 170, pp. 575-581
  • Venkatesh, B., Kirkness, E.F., Loh, Y.H., Halpern, A.L., Lee, A.P., Johnson, J., Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome (2007) PLoS Biol, 5
  • Venkatesh, B., Lee, A.P., Ravi, V., Maurya, A.K., Lian, M.M., Swann, J.B., Elephant shark genome provides unique insights into gnathostome evolution (2014) Nature, 505, pp. 174-179
  • Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., Zhang, Y., The I-TASSER Suite: protein structure and function prediction (2015) Nat. Methods, 12, pp. 7-8
  • Yun, S., Furlong, M., Sim, M., Cho, M., Park, S., Cho, E.B., Prevertebrate local gene duplication facilitated expansion of the neuropeptide GPCR superfamily (2015) Mol. Biol. Evol, 32, pp. 2803-2817

Citas:

---------- APA ----------
Gaillard, A.-L., Tay, B.-H., Sirkin, D.I.P., Lafont, A.-G., De Flori, C., Vissio, P.G., Mazan, S.,..., Tostivint, H. (2018) . Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives. Frontiers in Neuroscience, 12(SEP).
http://dx.doi.org/10.3389/fnins.2018.00607
---------- CHICAGO ----------
Gaillard, A.-L., Tay, B.-H., Sirkin, D.I.P., Lafont, A.-G., De Flori, C., Vissio, P.G., et al. "Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives" . Frontiers in Neuroscience 12, no. SEP (2018).
http://dx.doi.org/10.3389/fnins.2018.00607
---------- MLA ----------
Gaillard, A.-L., Tay, B.-H., Sirkin, D.I.P., Lafont, A.-G., De Flori, C., Vissio, P.G., et al. "Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives" . Frontiers in Neuroscience, vol. 12, no. SEP, 2018.
http://dx.doi.org/10.3389/fnins.2018.00607
---------- VANCOUVER ----------
Gaillard, A.-L., Tay, B.-H., Sirkin, D.I.P., Lafont, A.-G., De Flori, C., Vissio, P.G., et al. Characterization of gonadotropin-releasing hormone (GnRH) genes from cartilaginous fish: Evolutionary perspectives. Front. Neurosci. 2018;12(SEP).
http://dx.doi.org/10.3389/fnins.2018.00607