Coevolution of the spexin/galanin/kisspeptin family: Spexin activates galanin receptor type II and III

Endocrinology

Volumn 155, Issue 5, 2014, Pages 1864-1873

  Kim, Dong Kyu ^a   Yun, Seongsik ^a   Son, Gi Hoon ^a   Hwang, Jong Ik ^a   Park, Cho Rong ^a   Kim, Jae Il ^b   Kim, Kyungjin ^c   Vaudry, Hubert ^d   Seong, Jae Young ^a  

^a Korea University College of Medicine   (South Korea)

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

^c Seoul National University   (South Korea)

^d UNIVERSITÉ DE ROUEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GALANIN; GALANIN RECEPTOR 1; GALANIN RECEPTOR 2; GALANIN RECEPTOR 3; KISSPEPTIN; NEUROPEPTIDE; SPEXIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANOLIS; ARTICLE; BINDING AFFINITY; CHICKEN; COELACANTH; COEVOLUTION; DEUTEROSTOMIA; DROSOPHILA; ENZYME ACTIVATION; EXON; GENE DUPLICATION; GENE LINKAGE GROUP; GENE STRUCTURE; GENOMIC FRAGMENT; HUMAN; HUMAN CELL; HUMAN CHROMOSOME; NONHUMAN; ORYZIAS; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SEQUENCE ALIGNMENT; VERTEBRATE; XENOPUS; XENOPUS TROPICALIS; ZEBRA FISH;

ANIMALS; CHROMOSOME MAPPING; DATABASES, NUCLEIC ACID; DATABASES, PROTEIN; EVOLUTION, MOLECULAR; GALANIN; GENE DUPLICATION; HEK293 CELLS; HUMANS; KISSPEPTINS; LIGANDS; NEUROPEPTIDES; PEPTIDE HORMONES; PHYLOGENY; PROTEIN ISOFORMS; RECEPTOR, GALANIN, TYPE 1; RECEPTOR, GALANIN, TYPE 2; RECEPTOR, GALANIN, TYPE 3; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SYNTENY; ZEBRAFISH PROTEINS;

EID: 84899432079     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-2106     Document Type: Article

References (47)

1. Mirabeau O, Perlas E, Severini C, et al. Identification of novel peptide hormones in the human proteome by hidden Markov model screening. Genome Res. 2007;17:320-327
2. Sonmez K, Zaveri NT, Kerman IA, et al. Evolutionary sequence modeling for discovery of peptide hormones. PLoS Comput Biol. 2009;5:e1000258
3. Wan B, Wang XR, Zhou YB, Zhang X, Huo K, Han ZG. C12ORF39, a novel secreted protein with a typical amidation processing signal. Biosci Rep. 2010;30:1-10
4. Liu Y, Li S, Qi X, et al. A novel neuropeptide in suppressing luteinizing hormone release in goldfish, Carassius auratus. Mol Cell Endocrinol. 2013;374:65-72
5. Wong MK, Sze KH, Chen T, et al. Goldfish spexin: solution structure and novel function as a satiety factor in feeding control. Am J Physiol Endocrinol Metab. 2013;305:E348-E366
6. Porzionato A, Rucinski M, Macchi V, Stecco C, Malendowicz LK, De Caro R. Spexin expression in normal rat tissues. J Histochem Cytochem. 2010;58:825-837
7. Rucinski M, Porzionato A, Ziolkowska A, et al. Expression of the spexin gene in the rat adrenal gland and evidences suggesting that spexin inhibits adrenocortical cell proliferation. Peptides. 2010;31: 676-682
8. Porzionato A, RucinskiM,Macchi V, et al. Spexin is expressed in the carotid body and is upregulated by postnatal hyperoxia exposure. Adv Exp Med Biol. 2012;758:207-213
9. Toll L, Khroyan TV, Sonmez K, et al. Peptides derived from the prohormone proNPQ/spexin are potent central modulators of cardiovascular and renal function and nociception. FASEB J. 2012;26: 947-954
10. Fredriksson R, Lagerström MC, Lundin LG, Schiöth HB. The Gprotein- coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol. 2003;63:1256-1272
11. Larsson TA, Olsson F, Sundstrom G, et al. Early vertebrate chromosome duplications and the evolution of the neuropeptide Y receptor gene regions. BMC Evol Biol. 2008;8:184
12. Lee YR, Tsunekawa K, Moon MJ, et al. Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology. 2009;150:2837-2846
13. Kim DK, Cho EB, Moon MJ, et al. Revisiting the evolution of gonadotropin- releasing hormones and their receptors in vertebrates: secrets hidden in genomes. Gen Comp Endocrinol. 2011;170:68-78
14. Hwang JI, Moon MJ, Park S, et al. Expansion of secretin-like G protein-coupled receptors and their peptide ligands via local duplications before and after two rounds of whole-genome duplication. Mol Biol Evol. 2013;30:1119-1130
15. Yegorov S, Good S. Using paleogenomics to study the evolution of gene families: origin and duplication history of the relaxin family hormones and their receptors. PLoS One. 2012;7:e32923
16. Lee DK, Nguyen T, O'Neill GP, et al. Discovery of a receptor related to the galanin receptors. FEBS Lett. 1999;446:103-107
17. Nakatani Y, Takeda H, Kohara Y, Morishita S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 2007;17:1254-1265
18. Conklin BR, Farfel Z, Lustig KD, Julius D, Bourne HR. Substitution of three amino acids switches receptor specificity of Gq α to that of Gi α. Nature. 1993;363:274-276
19. Moon MJ, Kim HY, Park S, et al. Evolutionarily conserved residues at glucagon-like peptide-1 (GLP-1) receptor core confer ligand-induced receptor activation. J Biol Chem. 2012;287:3873-3884
20. Carpenter KA, Schmidt R, Yue SY, et al. The glycine residue in cyclic lactam analogues of galanin(1-16)-NH2 is important for stabilizing an N-terminal helix. Biochemistry. 1999;38:15295-15304
21. Um HN, Han JM, Hwang JI, Hong SI, Vaudry H, Seong JY. Molecular coevolution of kisspeptins and their receptors from fish to mammals. Ann NY Acad Sci. 2010;1200:67-74
22. Pasquier J, Lafont AG, Tostivint H, Vaudry H, Rousseau K, Dufour S. Comparative evolutionary histories of kisspeptins and kisspeptin receptors in vertebrates reveal both parallel and divergent features. Front Endocrinol (Lausanne). 2012;3:173
23. Liu Z, Xu Y, Wu L, Zhang S. Evolution of galanin receptor genes: insights from the deuterostome genomes. J Biomol Struct Dyn. 2010;28:97-106
24. Lenz C, Søndergaard L, Grimmelikhuijzen CJ. Molecular cloning and genomic organization of a novel receptor from Drosophila melanogaster structurally related to mammalian galanin receptors. Biochem Biophys Res Commun. 2000;269:91-96
25. Bendena WG, Boudreau JR, Papanicolaou T, Maltby M, Tobe SS, Chin-Sang ID. A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues. Proc Natl Acad Sci USA. 2008;105:1339-1342
26. Webling KE, Runesson J, Bartfai T, Langel U. Galanin receptors and ligands. Front Endocrinol (Lausanne). 2012;3:146
27. Cardoso JC, Vieira FA, Gomes AS, Power DM. The serendipitous origin of chordate secretin peptide family members.BMCEvol Biol. 2010;10:135
28. Neumann JM, Couvineau A, Murail S, Lacapère JJ, Jamin N, LaburtheM. Class-BGPCRactivation: is ligand helix-capping the key? Trends Biochem Sci. 2008;33:314-319
29. Castellano JM, Navarro VM, Fernández-Fernández R, et al. Effects of galanin-like peptide on luteinizing hormone secretion in the rat: sexually dimorphic responses and enhanced sensitivity at male puberty. Am J Physiol Endocrinol Metab. 2006;291:E1281-E1289
30. Taylor A, Madison FN, Fraley GS. Galanin-like peptide stimulates feeding and sexual behavior via dopaminergic fibers within the medial preoptic area of adult male rats. J Chem Neuroanat. 2009;37: 105-111
31. Choe HK, Kim HD, Park SH, et al. Synchronous activation of gonadotropin- releasing hormone gene transcription and secretion by pulsatile kisspeptin stimulation. Proc Natl Acad Sci USA. 2013; 110:5677-5682
32. Roseweir AK, Kauffman AS, Smith JT, et al. Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation. J Neurosci. 2009;29:3920-3929
33. Messager S, Chatzidaki EE, Ma D, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release viaGprotein-coupled receptor 54. Proc Natl Acad Sci USA. 2005;102:1761-1766
34. Waters SM, Krause JE. Distribution of galanin-1, -2 and -3 receptor messengerRNAsin central and peripheral rat tissues. Neuroscience. 2000;95:265-271
35. Mitchell V, Bouret S, Prévot V, Jennes L, Beauvillain JC. Evidence for expression of galanin receptor Gal-R1 mRNA in certain gonadotropin releasing hormone neurones of the rostral preoptic area. J Neuroendocrinol. 1999;11:805-812
36. Mitchell V, Bouret S, Howard AD, Beauvillain JC. Expression of the galanin receptor subtype Gal-R2 mRNA in the rat hypothalamus. J Chem Neuroanat. 1999;16:265-277
37. Kalló I, Vida B, Deli L, et al. Co-localisation of kisspeptin with galanin or neurokinin B in afferents to mouse GnRH neurones. J Neuroendocrinol. 2012;24:464-476
38. Tillet Y, Tourlet S, Picard S, Sizaret PY, Caraty A. Morphofunctional interactions between galanin and GnRH-containing neurones in the diencephalon of the ewe. The effect of oestradiol. J Chem Neuroanat. 2012;43:14-19
39. Shiba K, Kageyama H, Takenoya F, Shioda S. Galanin-like peptide and the regulation of feeding behavior and energy metabolism.FEBS J. 2010;277:5006-5013
40. Stengel A, Wang L, Goebel-Stengel M, Taché Y. Centrally injected kisspeptin reduces food intake by increasing meal intervals in mice. Neuroreport. 2011;22:253-257
41. Luque RM, Kineman RD, Tena-Sempere M. Regulation of hypothalamic expression of KiSS-1 and GPR54 genes by metabolic factors: analyses using mouse models and a cell line. Endocrinology. 2007;148:4601-4611
42. Mazarati A, Lu X, Kilk K, Langel U, Wasterlain C, Bartfai T. Galanin type 2 receptors regulate neuronal survival, susceptibility to seizures and seizure-induced neurogenesis in the dentate gyrus. Eur J Neurosci. 2004;19:3235-3244
43. Qi Y, Henry BA, Oldfield BJ, Clarke IJ. The action of leptin on appetite-regulating cells in the ovine hypothalamus: demonstration of direct action in the absence of the arcuate nucleus. Endocrinology. 2010;151:2106-2116
44. Badie-Mahdavi H, Lu X, Behrens MM, Bartfai T. Role of galanin receptor 1 and galanin receptor 2 activation in synaptic plasticity associated with 3',5'-cyclic AMP response element-binding protein phosphorylation in the dentate gyrus: studies with a galanin receptor 2 agonist and galanin receptor 1 knockout mice. Neuroscience. 2005;133:591-604
45. Bailey KR, Pavlova MN, Rohde AD, Hohmann JG, Crawley JN. Galanin receptor subtype 2 (GalR2) null mutant mice display an anxiogenic-like phenotype specific to the elevated plus-maze. Pharmacol Biochem Behav. 2007;86:8-20
46. Liu HX, Brumovsky P, Schmidt R, et al. Receptor subtype-specific pronociceptive and analgesic actions of galanin in the spinal cord: selective actions via GalR1 and GalR2 receptors. Proc Natl Acad Sci USA. 2001;98:9960-9964
47. Swanson CJ, Blackburn TP, Zhang X, et al. Anxiolytic- and antidepressant- like profiles of the galanin-3 receptor (Gal3) antagonists SNAP 37889 and SNAP 398299. Proc Natl Acad Sci USA. 2005;102:17489-17494.