Identification of two isoforms of the kisspeptin-1 receptor (kiss1r) generated by alternative splicing in a modern teleost, the senegalese sole (solea senegalensis)

Biology of Reproduction

Volumn 80, Issue 1, 2009, Pages 60-69

  Mechaly, Alejandro S ^a   Viñas, Jordi ^a   Piferrer, Francesc ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

Alternative splicing; Brain; Fish model; GPR54; Kiss1r; Kisspeptin; Kisspeptin receptor; Kisspeptin 1 receptor; Neuroendocrinology; Puberty; Senegalese sole; Solea senegalensis; Teleost

Indexed keywords

AMINO ACID; COMPLEMENTARY DNA; G PROTEIN COUPLED RECEPTOR 54; GENOMIC DNA; ISOPROTEIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CODON; DATA BASE; FEMALE; GENETIC TRANSCRIPTION; GONAD; INTRON; MALE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN VARIANT; PUBERTY; SIGNAL TRANSDUCTION; SOLEA SENEGALENSIS; STOP CODON; TELEOST;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; FEMALE; FLATFISHES; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN ISOFORMS; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ALIGNMENT;

SOLEA SENEGALENSIS; TELEOSTEI; VERTEBRATA;

EID: 58149485345     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.072173     Document Type: Article

References (54)

1. Lee DK, Nguyen T, O'Neill GP, Cheng R, Liu Y, Howard AD, Coulombe N, Tan CP, Tang-Nguyen AT, George SR, O'Dowd BF. Discovery of a receptor related to the galanin receptors. Febs Letters 1999; 446:103-107.
2. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CGC, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 2001; 276:28969-28975.
3. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001; 411:613-617.
4. Kotani M, Detheux M, Vandenbbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suárez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001; 276:34631-34636.
5. Smith JT, Clifton DK, Steiner RA. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 2006;131:623-630.
6. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum Reprod Update 2006; 12:631-639.
7. Messager S. Kisspeptin and its receptor: new gatekeepers of puberty. J Neuroendocrinol 2005; 17:687-688.
8. Dungan HM, Clifton DK, Steiner RA. Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 2006; 147:1154-1158.
9. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang SJ, Monsma FJ, Gustafson EL. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003; 312:1357-1363.
10. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003; 100:10972-10976.
11. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MBL, Crowley WF, Aparicio SAJR, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349:1614-1618.
12. Mead EJ, Maguire JJ, Kuc RE, Davenport AP. Kisspeptins are novel potent vasoconstrictors in humans, with a discrete localization of their receptor, G protein-coupled receptor 54, to atherosclerosis-prone vessels. Endocrinology 2007; 148:140-147.
13. Hauge-Evans AC, Richardson CC, Milne HM, Christie MR, Persaud SJ, Jones PM. A role for kisspeptin in islet function. Diabetologia 2006; 49:2131-2135.
14. Bilban M, Ghaffari-Tabrizi N, Hintermann E, Bauer S, Molzer S, Zoratti C, Malli R, Sharabi A, Hiden U, Graier W, Knofler M, Andreae F, Wagner O, Quaranta V, Desoye G. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci 2004; 117:1319-1328.
15. Stafford LJ, Xia CZ, Ma WB, Cai Y, Liu MY. Identification and characterization of mouse metastasis-suppressor KiSS1 and its G-protein-coupled receptor. Cancer Res 2002; 62:5399-5404.
16. Clements MK, McDonald TP, Wang RP, Xie GC, O'Dowd BF, George SR, Austin CP, Liu QY. FMRFamide-related neuropeptides are agonists of the orphan G-protein-coupled receptor GPR54. Biochem Biophys Res Commun 2001; 284:1189-1193.
17. van Aerle R, Kille P, Lange A, Tyler CR. Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish. Peptides 2008; 29:57-64.
18. Kanda S, Akazome Y, Matsunaga T, Yamamoto N, Yamada S, Tsukamura H, Maeda KI, Oka Y. Identification of kiss-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in Medaka (Oryzias latipes). Endocrinology 2008; 149:2467-2476.
19. Parhar IS, Ogawa S, Sakuma Y. Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel g protein-coupled receptor (gpr54) during maturation in cichlid fish. Endocrinology 2004; 145:3613-3618.
20. Parhar IS. GnRH and gpr: laser-captured single cell gene profiling. Fish Physiol Biochem 2005; 31:153-156.
21. Mohamed JS, Benninghoff AD, Holt GJ, Khan IA. Developmental expression of the G protein-coupled receptor 54 and three GnRH mRNAs in the teleost fish cobia. J Mol Endocrinol 2007; 38:235-244.
22. Nocillado JN, Levavi-Sivan B, Carrick F, Elizur A. Temporal expression of G-protein-coupled receptor 54 (GPR54) gonadotropin-releasing hormones (GnRH), and dopamine receptor D2 (drd2) in pubertal female grey mullet, Mugil cephalus. Gen Comp Endocrinol 2007; 150:278-287.
23. Filby AL, van Aerle R, Duitman J, Tyler CR. The kisspeptin/gonadotropin- releasing hormone pathway and molecular signaling of puberty in fish. Biol Reprod 2008; 78:278-289.
24. Biran J, Ben-Dor S, Levavi-Sivan B. Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol Reprod 2008; 79:776-786.
25. Nelson NJ. Fishes of the World, 4th ed. Hoboken, New Jersey: John Wiley & Sons, Inc; 2006:442-451.
26. Imsland AK, Foss A, Conceicao LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P. A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fish 2003; 13:379-407.
27. Anguis V, Cañavate JP. Spawning of captive Senegal sole (Solea senegalensis) under a naturally fluctuating temperature regime. Aquacul-ture 2005; 243:133-145.
28. García-López A, Martínez-Rodríguez G, Sarasquete C. Male reproductive system in Senegalese sole Solea senegalensis (Kaup): anatomy, histology and histochemistry. Histol Histopath 2005; 20:1179-1189.
29. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999;41:95-98.
30. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 1994; 22:4673-4680.
31. Saitou N, Nei M. The neighbor-joining method-a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406-425.
32. Felsenstein J. Confidence limits on phylogenies-an approach using the bootstrap. Evolution 1985; 39:783-791.
33. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007; 24:1596-1599.
34. García-López A, Anguis V, Couto E, Canario AVM, Cañavate JP, Sarasquete C, Martínez-Rodríguez G. Non-invasive assessment of reproductive status and cycle of sex steroid levels in a captive wild broodstock of Senegalese sole Solea senegalensis (Kaup). Aquaculture 2006; 254:583-593.
35. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000;25:169-193.
36. Lewis D, Freeman DA, Dark J, Wynne-Edwards KE, Zucker I. Photoperiodic control of oestrous cycles in Syrian hamsters: mediation by the mediobasal hypothalamus. J Neuroendocrinol 2002; 14:605.
37. Baldwin JM. Structure and function of receptors coupled to G-proteins. Curr Opin Cell Biol 1994; 6:180-190.
38. Moon JS, Lee YR, Oh DY, Hwang JI, Lee JY, Kim J, Vaudry H, Kwon HB, Seong Y. Molecular cloning of the bullfrog kisspeptin receptor Gpr54 with high sensitivity to Xenopus kisspeptin. Peptides 2008; (in press). published online ahead of print 4 May 2008; DOI:10.1016/j.peptides.2008.1004.1015.
39. Smith CWJ, Valcái rcel J. Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci 2000; 25:381-388.
40. Ast G. How did alternative splicing evolve? Nat Rev Genet 2004; 5:773-782.
41. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003; 72:291-336.
42. Izquierdo JM, Valcái rcel J. A simple principle to explain the evolution of pre-mRNA splicing. Genes Dev 2006; 20:1679-1684.
43. Matlin AJ, Clark F, Smith CW. Understanding alternative splicing:towards a cellular code. Nat Rev Mol Cell Biol 2005; 6:386-398.
44. Kilpatrick GJ, Dautzenberg FM, Martin GR, Eglen RM. 7TM receptors:the splicing on the cake. Trends Pharmacol Sci 1999; 20:294-301.
45. Fradinger EA, Tello JA, Rivier JE, Sherwood NM. Characterization of four receptor cDNAs: PAC(1), VPAC(1), a novel PAC(1) and a partial GHRH in zebrafish. Mol Cel Endocrinol 2005; 231:49-63.
46. Hashimoto K, Koga M, Motomura T, Kasayama S, Kouhara H, Ohnishi T, Arita N, Hayakawa T, Sato B, Kishimoto T. Identification of alternatively spliced messenger-ribonucleic-acid encoding truncated growth hormone-releasing hormone-receptor in human pituitary adenomas. J Clin Endocrinol Metab 1995; 80:2933-2939.
47. Horikawa R, Gaylinn BD, Lyons CE, Thorner MO. Molecular cloning of ovine and bovine growth hormone-releasing hormone receptors: the ovine receptor is C-terminally truncated. Endocrinology 2001; 142:2660-2668.
48. Minneman KP. Splice variants of G protein-coupled receptors. Mol Interv 2001; 1:108-116.
49. Gottsch ML, Clifton DK, Steiner RA. KISSPEPEPTIN-GPR54 signaling in the neuroendocrine reproductive axis. Mol Cell Endocrinol 2006; 254:91-96.
50. Lanfranco F, Gromoll J, von Eckardstein S, Herding EM, Nieschlag E, Simoni M. Role of sequence variations of the GnRH receptor and G protein-coupled receptor 54 gene in male idiopathic hypogonadotropic hypogonadism. Eur J Endocrinol 2005; 153:845-852.
51. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25:11349-11356.
52. Roa J, Vigo E, Castellano JM, Navarro VM, Fernáindez- Fernáindez R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 2006; 147:2864-2878.
53. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sáinchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004; 145:4565-4574.
54. Kauffman AS, Park JH, McPhie-Lalmansingh AA, Gottsch ML, Bodo C, Hohmann JG, Pavlova MN, Rohde AD, Clifton DK, Steiner RA, Rissman EF. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci 2007; 27:8826-8835.