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Abstract:

GnRH-associated peptide (GAP) is the C-terminal portion of the gonadotropin-releasing hormone (GnRH) preprohormone. Although it was reported in mammals that GAP may act as a prolactin-inhibiting factor and can be co-secreted with GnRH into the hypophyseal portal blood, GAP has been practically out of the research circuit for about 20 years. Comparative studies highlighted the low conservation of GAP primary amino acid sequences among vertebrates, contributing to consider that this peptide only participates in the folding or carrying process of GnRH. Considering that the three-dimensional (3D) structure of a protein may define its function, the aim of this study was to evaluate if GAP sequences and 3D structures are conserved in the vertebrate lineage. GAP sequences from various vertebrates were retrieved from databases. Analysis of primary amino acid sequence identity and similarity, molecular phylogeny, and prediction of 3D structures were performed. Amino acid sequence comparison and phylogeny analyses confirmed the large variation of GAP sequences throughout vertebrate radiation. In contrast, prediction of the 3D structure revealed a striking conservation of the 3D structure of GAP1 (GAP associated with the hypophysiotropic type 1 GnRH), despite low amino acid sequence conservation. This GAP1 peptide presented a typical helix-loop-helix (HLH) structure in all the vertebrate species analyzed. This HLH structure could also be predicted for GAP2 in some but not all vertebrate species and in none of the GAP3 analyzed. These results allowed us to infer that selective pressures have maintained GAP1 HLH structure throughout the vertebrate lineage. The conservation of the HLH motif, known to confer biological activity to various proteins, suggests that GAP1 peptides may exert some hypophysiotropic biological functions across vertebrate radiation. © 2017 Pérez Sirkin, Lafont, Kamech, Somoza, Vissio and Dufour.

Registro:

Documento: Artículo
Título:Conservation of three-dimensional helix-loop-helix structure through the vertebrate lineage reopens the cold case of gonadotropin-releasing hormone-associated Peptide
Autor:Pérez Sirkin, D.I.; Lafont, A.-G.; Kamech, N.; Somoza, G.M.; Vissio, P.G.; Dufour, S.
Filiación:Laboratorio de Neuroendocrinología del Crecimiento y la Reproducción, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Biodiversidad y Biología Experimental y Aplicada (IBBEA), Buenos Aires, Argentina
Muséum National d'Histoire Naturelle, Sorbonne Universités, UMR BOREA, Biologie des Organismes et Ecosystèmes Aquatiques, CNRS, IRD, UPMC, UNICAEN, UA, Paris, France
Instituto de Investigaciones Biotecnológicas-Instituto Tecnológico de Chascomús (CONICET-UNSAM), Chascomús, Argentina
Palabras clave:Evolution; GnRH-associated peptide; Helix-loop-helix; Phylogeny; Protein 3D structure; Teleosts; Vertebrates
Año:2017
Volumen:8
Número:AUG
Página de inicio:207
DOI: http://dx.doi.org/10.3389/fendo.2017.00207
Título revista:Frontiers in Endocrinology
Título revista abreviado:Front. Endocrinol.
ISSN:16642392
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_16642392_v8_nAUG_p207_PerezSirkin

Referencias:

  • Matsuo, H., Baba, Y., Nair, R.G., Arimura, A., Schally, A.V., Structure of the porcine LH-and FSH-releasing hormone. I. The proposed amino acid sequence (1971) Biochem Bioph Res Commun, 43 (6), pp. 1334-1339
  • Burgus, R., Butcher, M., Ling, N., Monahan, M., Rivier, J., Fellows, R., Molecular structure of the hypothalamic factor (LRF) of ovine origin monitoring thesecretion of pituitary gonadotropic hormone of luteinization (LH) (1971) C R Acad Sci Hebd Seances Acad Sci D, 273 (18), p. 1611
  • Fernald, R.D., White, R.B., Gonadotropin-releasing hormone genes: phylogeny, structure, and functions (1999) Front Neuroendocrinol, 20 (3), pp. 224-240
  • Guilgur, L.G., Moncaut, N.P., Canário, A.V., Somoza, G.M., Evolution of GnRH ligands and receptors in gnathostomata (2006) Comp Biochem Physiol A Mol Integr Physiol, 144 (3), pp. 272-283
  • Roch, G.J., Busby, E.R., Sherwood, N.M., GnRH receptors and peptides: skating backward (2014) Gen Comp Endocrinol, 209, pp. 118-134
  • 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 (1), pp. 68-78
  • Tostivint, H., Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations (2011) Gen Comp Endocrinol, 170 (3), pp. 575-581
  • Decatur, W.A., Hall, J.A., Smith, J.J., Li, W., Sower, S.A., Insight from the lamprey genome: glimpsing early vertebrate development via neuroendocrineassociated genes and shared synteny of gonadotropin-releasing hormone (GnRH) (2013) Gen Comp Endocrinol, 192, pp. 237-245
  • Plachetzki, D.C., Tsai, P.S., Kavanaugh, S.I., Sower, S.A., Ancient origins of metazoan gonadotropin-releasing hormone and their receptors revealed by phylogenomic analyses (2016) Gen Comp Endocrinol, 234, pp. 10-19
  • 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 (1), pp. 346-364
  • Miyamoto, K., Hasegawa, Y., Nomura, M., Igarashi, M., Kangawa, K., Matsuo, H., Identification of the second gonadotropin-releasing hormone in chicken hypothalamus: evidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species (1984) Proc Natl Acad Sci U S A, 81 (12), pp. 3874-3878
  • 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 (8), pp. 3860-3869
  • Pawson, A.J., Morgan, K., Maudsley, S.R., Millar, R.P., Type II gonadotrophin-releasing hormone (GnRH-II) in reproductive biology (2003) Reproduction, 126 (3), pp. 271-278
  • Morgan, K., Millar, R.P., Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species (2004) Gen Comp Endocr, 139 (3), pp. 191-197
  • Sherwood, N., Eiden, L., Brownstein, M., Spiess, J., Rivier, J., Vale, W., Characterization of a teleost gonadotropin-releasing hormone (1983) Proc Natl Acad Sci U S A, 80 (9), pp. 2794-2798
  • Silver, M.R., Kawauchi, H., Nozaki, M., Sower, S.A., Cloning and analysis of the lamprey GnRH-III cDNA from eight species of lamprey representing the three families of petromyzoniformes (2004) Gen Comp Endocrinol, 139 (1), pp. 85-94
  • Seeburg, P.H., Adelman, J.P., Characterization of cDNA for precursor of human luteinizing hormone releasing hormone (1984) Nature, 311, pp. 666-668
  • Nikolics, K., Mason, A.J., Szőnyi, É., Ramachandran, J., Seeburg, P.H., A prolactin-inhibiting factor within the precursor for human gonadotropin-releasing hormone (1985) Nature, 316 (6028), pp. 511-517
  • 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 Bioph Res Commun, 143 (2), pp. 665-671
  • Yu, W.H., Seeburg, P.H., Nikolics, K., McCann, S.M., Gonadotropin-releasing hormone-associated peptide exerts a prolactin-inhibiting and weak gonadotropin-releasing activity in vivo (1988) Endocrinology, 123 (1), pp. 390-395
  • Wormald, P.J., Millar, R.P., Kerdelhue, B., Substance P receptors in human pituitary: a potential inhibitor of luteinizing hormone secretion (1989) J Clin Endocrinol Metab, 69 (3), pp. 612-615
  • Chandrashekar, V., Bartke, A., Browning, R.A., Assessment of the effects of a synthetic gonadotropin-releasing hormone associated peptide on hormone release from the in situ and ectopic pituitaries in adult male rats (1988) Brain Res Bull, 21 (1), pp. 95-99
  • Yu, W.H., Arisawa, M., Millar, R.P., McCann, S.M., Effects of the gonadotropin-releasing hormone associated peptides (GAP) on the release ofluteinizing hormone (LH), follicle stimulating hormone (FSH) and prolactin (PRL) in vivo (1989) Peptides, 10 (6), pp. 1133-1138
  • Milton, S.C., Brandt, W.F., Schnölzer, M., Milton, R.C., Total solid-phase synthesis and prolactin-inhibiting activity of the gonadotropin-releasing hormone precursor protein and the gonadotropin-releasing hormone associated peptide (1992) Biochemistry, 31 (37), pp. 8799-8809
  • Kerrigan, J.R., Yasin, M., Haisenleder, D.J., Dalkin, A.C., Marshall, J.C., Regulation of gonadotropin subunit messenger ribonucleic acid expression in gonadotropin-releasing hormone (GnRH)-deficient female rats: effects of GnRH, galanin, GnRH-associated peptide, neuropeptide-Y, and thyrotropin-releasing hormone (1995) Biol Reprod, 53 (1), pp. 1-7
  • Chavali, G.B., Nagpal, S., Majumdar, S.S., Singh, O., Salunke, D.M., Helix-loop-helix motif in GnRH associated peptide is critical for negative regulation of prolactin secretion (1997) J Mol Biol, 272 (5), pp. 731-740
  • Ishibashi, M., Yamaji, T., Takaku, F., Teramoto, A., Fukushima, T., Toyama, M., Effect of GnRH-associated peptide on prolactin secretion from human lactotrope adenoma cells in culture (1987) Acta Endocrinol (Copenh), 116 (1), pp. 81-84
  • Thomas, G.B., Cummins, J.T., Doughton, B.W., Griffin, N., Millar, R.P., Milton, R., Gonadotropin-releasing hormone associated peptide (GAP) and putative processed GAP peptides do not release luteinizing hormone or follicle-stimulating hormone or inhibit prolactin secretion in the sheep (1988) Neuroendocrinology, 48 (4), pp. 342-350
  • Planas, J., Bern, H.A., Millar, R.P., Effects of GnRH-associated peptide and its component peptides on prolactin secretion from the tilapia pituitary in vitro (1990) Gen Comp Endocrinol, 77 (3), pp. 386-396
  • Barnett, D.K., Bunnell, T.M., Millar, R.P., Abbott, D.H., Gonadotropin-releasing hormone II stimulates female sexual behavior in marmoset monkeys (2006) Endocrinology, 147 (1), pp. 615-623
  • Matsuda, K., Nakamura, K., Shimakura, S.I., Miura, T., Kageyama, H., Uchiyama, M., Inhibitory effect of chicken gonadotropin-releasing hormone II on food intake in the goldfish, Carassius auratus (2008) Horm Behav, 54 (1), pp. 83-89
  • Millar, R.P., Pawson, A.J., Morgan, K., Rissman, E.F., Lu, Z.L., Diversity of actions of GnRHs mediated by ligand-induced selective signaling (2008) Front Neuroendocrinol, 29 (1), pp. 17-35
  • Okubo, K., Nagahama, Y., Structural and functional evolution of gonadotropin-releasing hormone in vertebrates (2008) Acta Physiol (Oxf), 193 (1), pp. 3-15
  • Oka, Y., Three types of gonadotrophin-releasing hormone neurones and steroid-sensitive sexually dimorphic kisspeptin neurones in teleosts (2009) J Neuroendocrinol, 21 (4), pp. 334-338
  • Sherwood, N.M., Parker, D.B., McRory, J.E., Lescheid, D.W., 1 molecular evolution of growth hormone-releasing hormone and gonadotropin-releasing hormone (1994) Fish Physiol, 13, pp. 3-66
  • Berg, J.M., Tymoczko, J.L., Gatto, G.J., (2015) Lubert Stryer. Biochemistry., , 8th ed (Chaps. I-2 and I-6). London, UK: Palgrave Macmillan
  • Sadowski, M.I., Jones, D.T., The sequence-structure relationship and protein function prediction (2009) Curr Opin Struct Biol, 19 (3), pp. 357-362
  • Edgar, R.C., MUSCLE: a multiple sequence alignment method with reduced time and space complexity (2004) BMC Bioinformatics, 5 (1), p. 113
  • Abascal, F., Zardoya, R., Posada, D., ProtTest: selection of best-fit models of protein evolution (2005) Bioinformatics, 21 (9), pp. 2104-2105
  • Stamatakis, A., Ott, M., Efficient computation of the phylogenetic likelihood function on multi-gene alignments and multi-core architectures (2008) Philos Trans R Soc Lond B Biol Sci, 363 (1512), pp. 3977-3984
  • 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 (1), pp. 7-8
  • Bond, C.T., Francis, R.C., Fernald, R.D., Adelman, J.P., Characterization of complementary DNA encoding the precursor for gonadotropin-releasinghormone and its associated peptide from a teleost fish (1991) Mol Endocrinol, 5 (7), pp. 931-937
  • Gupta, H.M., Salunke, D.M., Prolactin inhibiting factor has structural motif common to developmental-gene regulators (1992) Curr Sci India, 62, pp. 374-376
  • Liu, J., Shi, W., Warburton, D., A cysteine residue in the helix-loop-helix domain of Id2 is critical for homodimerization and function (2000) Biochem Bioph Res Commun, 273 (3), pp. 1042-1047
  • Illergard, K., Ardell, D.H., Elofsson, A., Structure is three to ten times more conserved than sequence – a study of structural response in protein cores (2009) Proteins, 77 (3), pp. 499-508
  • Sousounis, K., Haney, C.E., Cao, J., Sunchu, B., Tsonis, P.A., Conservation of the three-dimensional structure in non-homologous or unrelated proteins (2012) Hum Genomics, 6 (1), p. 10
  • Massari, M.E., Murre, C., Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms (2000) Mol Cell Biol, 20 (2), pp. 429-440
  • Leclerc, G.M., Boockfor, F.R., Pulses of prolactin promoter activity depend on a noncanonical E-box that can bind the circadian proteins CLOCK and BMAL1 (2005) Endocrinology, 146 (6), pp. 2782-2790
  • Resuehr, D., Wildemann, U., Sikes, H., Olcese, J., E-box regulation of gonadotropin-releasing hormone (GnRH) receptor expression in immortalized gonadotrope cells (2007) Mol Cell Endocrinol, 278 (1), pp. 36-43
  • Cherrington, B.D., Bailey, J.S., Diaz, A.L., Mellon, P.L., NeuroD1 and Mash1 temporally regulate GnRH receptor gene expression in immortalized mouse gonadotrope cells (2008) Mol Cell Endocrinol, 295 (1), pp. 106-114
  • Benezra, R., Davis, R.L., Lockshon, D., Turner, D.L., Weintraub, H., The protein Id: a negative regulator of helix-loop-helix DNA binding proteins (1990) Cell, 61 (1), pp. 49-59
  • Ellis, H.M., Spann, D.R., Posakony, J.W., Extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins (1990) Cell, 61 (1), pp. 27-38
  • Christy, B.A., Sanders, L.K., Lau, L.F., Copeland, N.G., Jenkins, N.A., Nathans, D., An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene (1991) Proc Natl Acad Sci U S A, 88 (5), pp. 1815-1819
  • Strynadka, N.C., James, M.N., Crystal structures of the helix-loop-helix calcium-binding proteins (1989) Ann Rev Biochem, 58 (1), pp. 951-999
  • Kretsinger, R.H., Nockolds, C.E., Carp muscle calcium-binding protein II. Structure determination and general description (1973) J Biol Chem, 248 (9), pp. 3313-3326
  • Vacher, P., Mariot, P., Dufy-Barbe, L., Nikolics, K., Seeburg, P.H., Kerdelhue, B., The gonadotropin-releasing hormone associated peptide reduces calcium entry in prolactin-secreting cells (1991) Endocrinology, 128 (1), pp. 285-294
  • Dufy-Barbe, L., Bresson, L., Vacher, P., Odessa, M.F., San Galli, F., Rive, J.J., Thyrotropin-releasing hormone and gonadotropin-releasing hormone-associated peptide modulation of [Ca'+]i in human lactotrophs (1993) Mol Cell Endocri, 95, pp. 67-74
  • Vân Chuoï, M., Vacher, P., Dufy, B., GnRH-associated peptide decreases cyclic AMP accumulation in the GH3 pituitary cell line (1993) Neuroendocrinology, 58 (2), pp. 251-257
  • Phillips, H.S., Nikolics, K., Branton, D., Seeburg, P.H., Immunocytochemical localization in rat brain of a prolactin release-inhibiting sequence of gonadotropin-releasing hormone prohormone (1985) Nature, 316 (6028), pp. 542-545
  • Chen, J., Li, G., Lu, J., Chen, L., Huang, Y., Wu, H., A novel type of PTD, common helix–loop–helix motif, could efficiently mediate protein transduction into mammalian cells (2006) Biochem Bioph Res Commun, 347 (4), pp. 931-940
  • Lim, S.K., Sandén, C., Selegård, R., Liedberg, B., Aili, D., Tuning liposome membrane permeability by competitive peptide dimerization and partitioning-folding interactions regulated by proteolytic activity (2016) Sci Rep, 6, p. 21123
  • Berridge, M.J., Lipp, P., Bootman, M.D., The versatility and universality of calcium signalling (2000) Nat Rev Mol Cell Bio, 1 (1), pp. 11-21
  • Peter, R.E., Yu, K.L., Marchant, T.A., Rosenblum, P.M., Direct neural regulation of the teleost adenohypophysis (1990) J Exp Zool A, 256 (S4), pp. 84-89
  • Gonzalez-Martinez, D., Zmora, N., Mañanos, E., Saligaut, D., Zanuy, S., Zohar, Y., Immunohistochemical localization of three different prepro-GnRHs in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides (2002) J Comp Neurol, 446 (2), pp. 95-113
  • Pandolfi, M., Cueto, J.A.M., Nostro, F.L.L., Downs, J.L., Paz, D.A., Maggese, M.C., GnRH systems of Cichlasoma dimerus (Perciformes, Cichlidae) revisited: a localization study with antibodies and riboprobes to GnRH-associated peptides (2005) Cell Tissue Res, 321 (2), pp. 219-232
  • Guilgur, L.G., Ortí, G., Strobl-Mazzulla, P.H., Fernandino, J.I., Miranda, L.A., Somoza, G.M., Characterization of the cDNAs encoding three GnRH forms in the pejerrey fish Odontesthes bonariensis (Atheriniformes) and the evolution of GnRH precursors (2007) J Mol Evol, 64 (6), pp. 614-627
  • Xia, W., Smith, O., Zmora, N., Xu, S., Zohar, Y., Comprehensive analysis of GnRH2 neuronal projections in zebrafish (2014) Sci Rep, 4, p. 3676
  • Ikemoto, T., Park, M.K., Molecular and evolutionary characterization of the GnRH-II gene in the chicken: distinctive genomic organization, expression pattern, and precursor sequence (2006) Gene, 368, pp. 28-36

Citas:

---------- APA ----------
Pérez Sirkin, D.I., Lafont, A.-G., Kamech, N., Somoza, G.M., Vissio, P.G. & Dufour, S. (2017) . Conservation of three-dimensional helix-loop-helix structure through the vertebrate lineage reopens the cold case of gonadotropin-releasing hormone-associated Peptide. Frontiers in Endocrinology, 8(AUG), 207.
http://dx.doi.org/10.3389/fendo.2017.00207
---------- CHICAGO ----------
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" . Frontiers in Endocrinology 8, no. AUG (2017) : 207.
http://dx.doi.org/10.3389/fendo.2017.00207
---------- MLA ----------
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" . Frontiers in Endocrinology, vol. 8, no. AUG, 2017, pp. 207.
http://dx.doi.org/10.3389/fendo.2017.00207
---------- VANCOUVER ----------
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. Front. Endocrinol. 2017;8(AUG):207.
http://dx.doi.org/10.3389/fendo.2017.00207