Gene structure analysis of kisspeptin-2 (Kiss2) in the Senegalese sole (Solea senegalensis): Characterization of two splice variants of Kiss2, and novel evidence for metabolic regulation of kisspeptin signaling in non-mammalian species

Molecular and Cellular Endocrinology

Volumn 339, Issue 1-2, 2011, Pages 14-24

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

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

Alternative splicing; Fasting; Kiss2; Kisspeptin 2; Puberty; Solea senegalensis

Indexed keywords

KISSPEPTIN; KISSPEPTIN 2; MESSENGER RNA; UNCLASSIFIED DRUG;

ADULT ANIMAL; ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GENE STRUCTURE; GONAD; MALE; METABOLIC REGULATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; SENEGALESE SOLE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TELEOST;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; CLONING, MOLECULAR; ENERGY METABOLISM; FEMALE; FISH PROTEINS; FLATFISHES; FOLLICLE STIMULATING HORMONE; FOOD DEPRIVATION; GENE COMPONENTS; GONADS; HYPOTHALAMUS; LUTEINIZING HORMONE; MALE; MOLECULAR SEQUENCE DATA; ORGAN SIZE; PHYLOGENY; PITUITARY GLAND; PROTEIN ISOFORMS; REPRODUCTION; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; STOMACH; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 79958074199     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.03.004     Document Type: Article

References (67)

1. Akazome Y., Kanda S., Okubo K., Oka Y. Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain. J. Fish. Biol. 2010, 76:161-182.
2. Aparicio S. Kisspeptins and GPR54 - the new biology of the mammalian GnRH axis. Cell. Metab. 2005, 1:293-296.
3. Arai A.C., Orwig N. Factors that regulate KiSS1 gene expression in the hippocampus. Brain Res. 2008, 1243:10-18.
4. Ben-Dov C., Hartmann B., Lundgren J., Valcárcel J.A. Genome-wide analysis of alternative Pre-mRNA splicing. J. Biol. Chem. 2008, 283:1229-1233.
5. 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.
6. Bowe J.E., King A.J., Kinsey-Jones J.S., Foot V.L., Li X.F., O'Byrne K.T., Persaud S.J., Jones P.M. Kisspeptin stimulation of insulin secretion: mechanisms of action in mouse islets and rats. Diabetologia 2009, 52:855-862.
7. Bustin S.A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 2000, 25:169-193.
8. Cardon M., Ron-Harel N., Cohen H., Lewitus G.M., Schwartz M. Dysregulation of kisspeptin and neurogenesis at adolescence link inborn immune deficits to the late onset of abnormal sensorimotor gating in congenital psychological disorders. Mol. Psychiatry 2009, 15:415-425.
9. Carrillo M., Zanuy S., Felip A., Bayarri M.J., Moles G., Gomez A. Hormonal and environmental control of puberty in perciform fish: the case of sea bass. Ann. N.Y. Acad. Sci. 2009, 1163:49-59.
10. Castellano J.M., Navarro V.M., Fernández-Fernández R., Nogueiras R., Tovar S., Roa J., Vazquez M.J., Vigo E., Casanueva F.F., Aguilar E., Pinilla L., Dieguez C., Tena-Sempere M. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 2005, 146:3917-3925.
11. Cerdà J., Chauvigné F., Agulleiro M.J., Marin E., Halm S., Martínez-Rodríguez G., Prat F. Molecular cloning of Senegalese sole (Solea senegalensis) follicle-stimulating hormone and luteinizing hormone subunits and expression pattern during spermatogenesis. Gen. Comp. Endocrinol. 2008, 156:470-481.
12. Cerdà-Reverter J.M., Sorbera L.A., Carrillo M., Zanuy S. Energetic dependence of NPY-induced LH secretion in a teleost fish (Dicentrarchus labrax). Am. J. Physiol. 1999, 227:1627-1634.
13. Costas B., Aragão C., Ruiz-Jarabo I., Vargas-Chacoff L., Arjona F.J., Dinis M.T., Mancera J.M., Conceição L.E. Feed deprivation in Senegalese sole (Solea senegalensis Kaup, 1858) juveniles: effects on blood plasma metabolites and free amino acid levels. Fish Physiol. Biochem. 2010, 10.1007/s10695-010-9451-2.
14. de Roux N. GnRH receptor and GPR54 inactivation in isolated gonadotropic deficiency. Horm. Res. Synth. 2006, 20:515-528.
15. Elizur A. The KiSS1/GPR54 system in fish. Peptides 2009, 30:164-170.
16. Felip A., Zanuy S., Pineda R., Pinilla L., Carrillo M., Tena-Sempere M., Gómez A. Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol. Cell. Endocrinol. 2009, 312:61-71.
17. Fernández-Fernández R., Martini A.C., Navarro V.M., Castellano J.M., Dieguez C., Aguilar E., Pinilla L., Tena-Sempere M. Novel signals for the integration of energy balance and reproduction. Mol. Cell. Endocrinol. 2006, 254-255:127-132.
18. Funes S., Hedrick J.A., Vassileva G., Markowitz L., Abbondanzo S., Golovko A., Yang S.J., Monsma F.J., Gustafson E.L. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem. Biophys. Res. Commun. 2003, 312:1357-1363.
19. Gaytan M., Castellano J.M., Roa J., Sanchez-Criado J.E., Tena-Sempere M., Gaytan F. Expression of KiSS-1 in rat oviduct: possible involvement in prevention of ectopic implantation?. Cell. Tissue Res. 2007, 329:571-579.
20. Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., Seminara S., Clifton D.K., Steiner R.A. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004, 145:4073-4077.
21. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999, 41:95-98.
22. Hiden U., Bilban M., Knöfler M., Desoye G. Kisspeptins and the placenta: regulation of trophoblast invasion. Rev. Endocr. Metab. Disord. 2007, 8:31-39.
23. Izquierdo J.M., Valcárcel J.A. Simple principle to explain the evolution of pre-mRNA splicing. Genes Dev. 2006, 20:1679-1684.
24. Kanda S., Akazome Y., Matsunaga T., Yamamoto N., Yamada S., Tsukamura H., Maeda K., Oka Y. Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 2008, 149:2467-2476.
25. Kimura M.A. Simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16:111-120.
26. Kitahashi T., Ogawa S., Parhar I.S. Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 2009, 150:821-831.
27. Kotani M., Detheux M., Vandenbbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., Brezillon S., Tyldesley R., Suarez-Huerta N., Vandeput F., Blanpain C., Schiffmann S.N., 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.
28. Lee J.H., Miele M.E., Hicks D.J., Phillips K.K., Trent J.M., Weissman B.E., Welch D.R. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J. Natl. Cancer Inst. 1996, 88:1731-1737.
29. Lee Y.R., Tsunekawa K., Moon M.J., Um H.N., Hwang J.I., Osugi T., Otaki N., Sunakawa Y., Kim K., Vaudry H., Kwon H.B., Seong J.Y., Tsutsui K. Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 2009, 150:2837-2846.
30. Li S., Zhang Y., Liu Y., Huang X., Huang W., Lu D., Zhu P., Shi Y., Cheng C.H., Liu X., Lin H. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J. Endocrinol. 2009, 201:407-418.
31. Lu J.G., Peatman E., Wang W.Q., Yang Q., Abernathy J., Wang S.L., Kucuktas H., Liu Z.J. Alternative splicing in teleost fish genomes: same-species and cross-species analysis and comparisons. Mol. Genet. Genomics 2010, 283:531-539.
32. Luque R.M., Kineman D., Tena-Sempere M. Regulation of hypothalamic expression of KiSS-1 and GPR54 genes by metabolic factors: Analysis using mouse models and a cell line. Endocrinology 2007, 148:4601-4611.
33. Makri A., Pissimissis N., Lembessis P., Polychronakos C., Koutsilieris M. The kisspeptin (KiSS1-1)/Gpr54 system in cancer biology. Cancer Treat. Rev. 2008, 34:682-692.
34. Matsui H., Takatsu Y., Kumano S., Matsumoto H., Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem. Biophys. Res. Commun. 2004, 320:383-388.
35. Mead E.J., Maguire J.J., Kuc R.E., Davenport A.P. 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.
36. Mechaly A.S., Viñas J., Piferrer F. Identification of two isoforms of the kisspeptin-1 receptor (kiss1r) generated by alternative splicing in a modern teleost, the Senegalese Sole (Solea senegalensis). Biol. Reprod. 2009, 80:60-69.
37. Mechaly A.S., Viñas J., Murphy C., Reith M., Piferrer F. Gene structure and regulation of the Kiss-1 receptor-2 (Kiss1r-2) in the Atlantic halibut: insights into the evolution and regulation of Kiss1r genes. Mol. Cell. Endocrinol. 2010, 317:78-89.
38. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., Thresher R.R., Malinge I., Lomet D., Carlton M.B.L., Colledge W.H., Caraty A., Aparicio S.A. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1761-1766.
39. Milla S., Wang N., Mandiki S.N.M., Kestemont P. Corticosteroids: friends or foes of teleost fish reproduction?. Comp. Biochem. Physiol. A 2009, 153:242-251.
40. Mitani Y., Kanda S., Akazome Y., Zempo B., Oka Y. Hypothalamic Kiss1 but not Kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes). Endocrinology 2010, 151:1751-1759.
41. Moon J.S., Lee Y.R., Oh D.Y., Hwang J.I., Lee J.Y., Kim J., Vaudry H., Kwon H.B., Seong Y. Molecular cloning of the bullfrog kisspeptin receptor Gpr54 with high sensitivity to Xenopus kisspeptin. Peptides 2009, 30:171-179.
42. Navarro V.M., Fernández-Fernández R., Castellano J.M., Roa J., Mayen A., Barreiro M.L., Gaytan F., Aguilar E., Pinilla L., Dieguez C., Tena-Sempere M. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J. Physiol. 2004, 561:379-386.
43. Oakley A.E., Clifton D.K., Steiner R.A. Kisspeptin signaling in the brain. Endocr. Rev. 2009, 30:713-743.
44. 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.
45. Parhar I.S., 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.
46. Popa S.M., Clifton D.K., Steiner R.A. The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction. Annu. Rev. Physiol. 2008, 70:213-238.
47. Roa J., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front. Neuroendocrinol. 2008, 29:48-69.
48. Roseweir A.K., Millar R.P. The role of kisspeptin in the control of gonadotrophin secretion. Hum. Reprod. Update 2009, 15:203-212.
49. Saitou N., Nei M. The Neighbor-Joining method -- a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
50. Selvaraj S., Kitano H., Fujinaga Y., Ohga H., Yoneda M., Yamaguchi A., Shimizu A., Matsuyama M. Molecular characterization, tissue distribution, and mRNA expression profiles of two Kiss genes in the adult male and female chub mackerel (Scomber japonicus) during different gonadal stages. Gen. Comp. Endocrinol. 2010, 169:28-38.
51. Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., Ojeda S.R., Plant T.M. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:2129-2134.
52. Shahjahan M., Motohashi E., Doi H., Ando H. Elevation of Kiss2 and its receptor gene expression in the brain and pituitary of grass puffer during the spawning season. Gen. Comp. Endocrinol. 2010, 169:48-57.
53. Shi Y., Zhang Y., Li S., Liu Q., Lu D., Liu M., Meng Z., Cheng C.H.K., Liu X., Lin H. Molecular identification of the Kiss2/Kiss1ra system and its potential function during 17alpha-methyltestosterone-induced sex reversal in the orange-spotted grouper, Epinephelus coloides. Biol. Reprod. 2010, 83:63-74.
54. Smith J.T., Acohido B.V., Clifton D.K., Steiner R.A. KiSS-1 neurons are direct targets for leptin in the ob/ob mouse. J. Neuroendocrinol. 2006, 18:298-303.
55. Smith E.M., Gregory T.R. Patterns of genome size diversity in the ray-finned fishes. Hydrobiologia 2009, 625:1-25.
56. 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.
57. Taranger G.L., Carrillo M., Schulz R.W., Fontaine P., Zanuy S., Felip A., Weltzien F.A., Dufour S., Karlsen O., Norberg B., Andersson E., Hansen T. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 2010, 165:483-515.
58. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum. Reprod. Update 2006, 12:631-639.
59. 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. Nucl. Acids Res. 1994, 22:4673-4680.
60. Unniappan S. Ghrelin: An emerging player in the regulation of reproduction in non-mammalian vertebrates. Gen. Comp. Endocrinol. 2010, 167:340-343.
61. Um H.N., Han J.M., Hwang J.I., Hong S.I., Vaudry H., Seong J.Y. Molecular coevolution of kisspeptins and their receptors from fish to mammals. Ann. N.Y. Acad. Sci. 2010, 1200:67-74.
62. van Aerle R., Kille P., Lange A., Tyler C.R. Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish. Peptides 2008, 29:57-64.
63. Volkoff H., Canosa L.F., Unniappan S., Cerdá-Reverter J.M., Bernier N.J., Kelly S.P., Peter R.E. Neuropeptides and the control of food intake in fish. Gen. Comp. Endocrinol. 2005, 142:3-19.
64. Volkoff H., Xu M., MacDonald E., Hoskins L. Aspects of the hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp. Biochem. Physiol. A 2009, 153:8-12.
65. Wahab F., Aziz F., Irfan S., Zaman W., Shahab M. Short-term fasting attenuates the response of the HPG axis to kisspeptin challenge in the adult male rhesus monkey (Macaca mulatta). Life Sci. 2008, 83:633-637.
66. Yang B., Jiang Q., Chan T., Ko W.K., Wong A.O. Goldfish kisspeptin: molecular cloning, tissue distribution of transcript expression, and stimulatory effects on prolactin, growth hormone and luteinizing hormone secretion and gene expression via direct actions at the pituitary level. Gen. Comp. Endocrinol. 2010, 165:60-71.
67. Zohar Y., Muñoz-Cueto J.A., Elizur A., Kah O. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 2009, 165:438-455.