Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals

Molecular and Cellular Endocrinology

Volumn 312, Issue 1-2, 2009, Pages 61-71

  Felip, Alicia ^a   Zanuy, Silvia ^a   Pineda, Rafael ^b   Pinilla, Leonor ^b   Carrillo, Manuel ^a   Tena Sempere, Manuel ^b   Gómez, Ana ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

^b UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Dicentrarchus labrax; Gonadotropins; KiSS 1; KiSS 2; Rattus norvegicus; Vertebrate evolution

Indexed keywords

FOLLITROPIN; GONADORELIN; KISSPEPTIN; KISSPEPTIN 10; KISSPEPTIN 2; LUTEINIZING HORMONE; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; COMPARATIVE STUDY; CONTROLLED STUDY; EUROPEAN SEA BASS; FEMALE; GENE DUPLICATION; GENE MAPPING; GENETIC CODE; GENETIC TRAIT; GONAD; HORMONE RELEASE; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; RAT; TELEOST; VERTEBRATE; ZEBRA FISH;

AGING; AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; BASS; CLONING, MOLECULAR; FEMALE; FISH PROTEINS; GONADOTROPINS, PITUITARY; MALE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; ORYZIAS; PHYLOGENY; PROTEINS; RATS; RATS, WISTAR; REPRODUCTION; SEASONS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SYNTENY; TIME FACTORS; VERTEBRATES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 70249145863     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.11.017     Document Type: Article

References (61)

1. Biran J., Ben-Dor S., and Levavi-Sivan B. Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol. Reprod. 79 (2008) 776-786
2. Briant C., Schneider J., Guillaume D., Ottogalli M., Duchamp G., Bruneau B., and Caraty A. Kisspeptin induces ovulation in cycling Welsh pony mares. Anim. Reprod. Sci. 94 (2006) 217-219
3. Brown R.E., Imran S.A., and Wilkinson E.Ur.M. KiSS-1 mRNA in adipose tissue is regulated by sex hormones and food intake. Mol. Cell. Endocrinol. 281 (2008) 64-72
4. Castellano J.M., Gaytan M., Roa J., Navarro V.M., Bellido C., Dieguez C., Aguilar E., Sánchez-Criado J.E., Pellicer A., Pinilla L., Gaytan F., and Tena-Sempere M. Expression of KiSS-1 in rat ovary: putative local regulator of ovulation?. Endocrinology 147 (2006) 4852-4862
5. Castellano J.M., Navarro V.M., Fernández-Fernández R., Castaño J.P., Malagón M.M., Aguilar E., Dieguez C., Magni P., Pinilla L., and Tena-Sempere M. Ontogeny and mechanisms of action for the stimulatory effect of kisspeptin on gonadotropin-releasing hormone system of the rat. Mol. Cell. Endocrinol. 257-258 (2006) 75-83
6. Castellano J.M., Navarro V.M., Fernández-Fernández R., Roa J., Vigo E., Pineda R., Dieguez C., Aguilar E., Pinilla L., and Tena-Sempere M. Expression of hypothalamic KiSS-1 system and rescue of defective gonadotropic responses by kisspeptin in streptozotocin-induced diabetic male rats. Diabetes 55 (2006) 2602-2610
7. Castellano J.M., Roa J., Luque R.M., Dieguez C., Aguilar E., Pinilla L., and Tena-Sempere M. KiSS-1/Kisspeptins and the metabolic control of reproduction; physiologic roles and putative physiopathological implications. Peptides (2008) 10.1016/j.peptides.2008.06.007
8. Colledge W.H. GPR54 and puberty. Trends Endocrinol. Metab. 15 (2004) 448-453
9. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., and Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 10972-10976
10. Dhillo W.S., Chaudhri O.B., Patterson M., Thompson E.L., Murphy K.G., Badman M.K., McGowan B.M., Amber V., Patel S., Ghatei M.A., and Bloom S.R. Kisspeptin-54 stimulates the hypothalamic-pituitary-gonadal axis in human males. J. Clin. Endocrinol. Metab. 90 (2005) 6609-6615
11. Dungan H.M., Clifton D.K., and Steiner R.A. Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 147 (2006) 1154-1158
12. Fernández-Fernández R., Martín A.C., Navarro V.M., Castellano J.M., Dieguez C., Aguilar E., Pinilla L., and Tena-Sempere M. Novel signals for the integration of energy balance and reproduction. Mol. Cell. Endocrinol. 254-255 (2006) 127-132
13. Filby A.L., van Aerle R., Duitman J.W., and Tyler C.R. The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol. Reprod. 78 (2008) 278-289
14. Gottsch M.L., Clifton D.K., and Steiner R.A. Kisspeptin-GPR54 signalling in the neuroendocrine reproductive axis. Mol. Cell. Endocrinol. 254-255 (2006) 91-96
15. Hofmann H.A. Gonadotropin-releasing hormone signalling in behavioral plasticity. Curr. Opin. Neurobiol. 16 (2006) 343-350
16. Horikoshi Y., Matsumoto H., Takatsu Y., Ohtaki T., Kitada C., Usuki S., and Fujino M. Dramatic elevation of plasma metastin concentrations in human pregnancy: metastin as a novel placenta-derived hormone in humans. J. Clin. Endocrinol. Metab. 88 (2003) 914-919
17. Hules M. Gene duplication: the genomic trade in spare parts. PloS Biol. 2 (2004) 900-904
18. Kaiser U.B., and Kuohung W. KiSS-1 and GPR54 as new players in gonadotropin regulation and puberty. Endocrine 26 (2005) 277-284
19. Kanda S., Akazome Y., Matsunaga T., Yamamoto N., Yamada S., Tsukamura H., Maeda K., and Oka Y. Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 149 (2008) 2467-2476
20. Kinoshita M., Tsukamura H., Adachi S., Matsui H., Uenoyama Y., Iwata K., Yamada S., Inoue K., Ohtaki T., Matsumoto H., and Maeda K.I. Involvement of central metastin in the regulation of preovulatory LH surge and estrous cyclicity in female rats. Endocrinology 146 (2005) 4431-4436
21. Luque R.M., Kineman R.D., and 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 148 (2007) 4601-4611
22. Mateos J., Mañanós E., Swanson P., Carrillo M., and Zanuy S. Purification of luteinizing hormone (LH) in the sea bass (Dicentrarchus labrax L.) and development of specific immunoassay (ELISA). Cienc. Mar. 32 (2006) 271-283
23. Matsui H., Takatsu Y., Kumano S., Matsumoto H., and Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem. Biophys. Res. Commun. 320 (2004) 383-388
24. Mead E.J., Maguire J.J., Kuc R.E., and 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 148 (2007) 140-147
25. Mechaly A.S., Viñas J., and 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. (2008) 10.1095/biolreprod.108.072173
26. 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., and Aparicio S.A.J.R. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 1761-1766
27. Meyer A., and Van de Peer Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27 (2005) 937-945
28. Mohamed J.S., Benninghoff A.D., Holt G.J., and Khan I.A. Developmental expression of the G protein-coupled receptor 54 and three GnRH mRNAs in the teleost fish cobia. J. Mol. Endocrinol. 38 (2007) 235-244
29. Molés G., Gómez A., Rocha A., Carrillo M., and Zanuy S. Purification and characterization of follicle-stimulating hormone from pituitary glands of sea bass (Dicentrarchus labrax). Gen. Comp. Endocrinol. 158 (2008) 68-76
30. Moon J.S., Lee Y.R., Oh D.Y., Hwang J.I., Lee J.Y., Kim J.I., Vaudry H., Kwon H.B., and Seong J.Y. Molecular cloning of the bullfrog kisspeptin receptor GPR54 with high sensitivity to Xenopus kisspeptin. Peptides (2008) 10.1016/j.peptides.2008.04.015
31. Murphy K.G. Kisspeptins: regulators of metastasis and the hypothalamic-pituitary-gonadal axis. J. Neuroendocrinol. 17 (2005) 519-525
32. Nakatani Y., Takeda H., Kohara Y., and Morishita S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 17 (2007) 1254-1265
33. Navarro V.M., Castellano J.M., Fernández-Fernández R., Barreiro M.L., Roa J., Sanchez-Criado J.E., Aguilar E., Dieguez C., Pinilla L., and 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 145 (2004) 4565-4574
34. Navarro V.M., Castellano J.M., Fernández-Fernández R., Tovar S., Roa J., Mayen A., Barreiro M.L., Casanueva F.F., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 146 (2005) 1689-1697
35. Navarro V.M., Castellano J.M., Fernández-Fernández R., Tovar S., Roa J., Mayen A., Nogueiras R., Vazquez M.J., Barreiro M.L., Magni P., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146 (2005) 156-163
36. Navarro V.M., Fernández-Fernández R., Castellano J.M., Roa J., Mayen A., Barreiro M.L., Gaytan F., Aguilar E., Pinilla L., Dieguez C., and Tena-Sempere M. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J. Physiology. 561 (2004) 379-386
37. Nocillado J.N., Levavi-Sivan B., Carrick F., and Elizur A. Temporal expression of G-protein-coupled receptor 54 (GPR54), gonadotropin-releasing hormones (GnRH), and dopamine receptor D2 (drd2) in pubertal female gray mullet, Mogul cephalous. Gen. Comp. Endocrinol. 150 (2007) 278-287
38. Okuzawa K. Puberty in teleosts. Fish Physiology. Biochem. 26 (2002) 31-41
39. Parhar I.S., Ogawa S., and 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 145 (2004) 3613-3618
40. Plant T.M., Ramaswamy S., and DiPietro M.J. Repetitive activation of hypothalamic GPR54 with intravenous pulses of kisspeptin in the juvenile monkey (Macaca mulatta) elicits a sustained train of GnRH discharges. Endocrinology 147 (2006) 1007-1013
41. Proudman J.A., Scanes C.G., Johannsen S.A., Berghman L.R., and Camp M.J. Comparison of the ability of the three endogenous GnRHs to stimulate release of follicle-stimulating hormone and luteinizing hormone in chickens. Domest. Anim. Endocrinol. 31 (2006) 141-153
42. Roa J., Aguilar E., Dieguez C., Pinilla L., and Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front. Neuroendocrinol. 29 (2008) 48-69
43. Roa J., and Tena-Sempere M. KiSS-1 system and reproduction: comparative aspects and roles in the control of female gonadotropic axis in mammals. Gen. Comp. Endocrinol. 153 (2007) 132-140
44. Rocha A., Gómez A., Zanuy S., Cerdá-Reverter J.M., and Carrillo M. Molecular characterization of two sea bass gonadotropin receptors: cDNA cloning, expression analysis, and functional activity. Mol. Cell. Endocrinol. 272 (2007) 63-76
45. Seminara S.B. Metastin and its G protein-coupled receptor, GPR54: critical pathway modulating GnRH secretion. Front. Neuroendocrinol. 26 (2005) 131-138
46. Seminara S.B., and Kaiser U.B. New gatekeepers of reproduction: GPR54 and its cognate ligand, KiSS-1. Endocrinology 146 (2005) 1686-1688
47. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno J.S., Shagoury J.K., Bo-Abbas Y., Kuohung W., Schwinof K.M., Hendrick A.G., Zahn D., Dixon J., Kaiser U.B., Slaugenhaupt S.A., Gusella J.F., O′Rahilly S., Carlton M.B.L., Crowley W.F., Aparicio S.A., and Colledge W.H. The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 349 (2003) 1614-1627
48. Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., and Ojeda S.R. Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 2129-2134
49. Shibata M., Friedman R.L., Ramaswamy S., and Plant T.M. Evidence that down regulation of hypothalamic KiSS-1 expression is involved in the negative feedback action of testosterone to regulate luteinising hormone secretion in the adult male rhesus monkey (Macaca mulatta). J. Neuroendocrinol. 19 (2007) 432-438
50. Smith J.T. Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe. Brain Res. Rev. 57 (2008) 288-298
51. Smith J.T., Acohido B.V., Clifton D.K., and Steiner R.A. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J. Neuroendocrinol. 18 (2006) 298-303
52. Smith J.T., Clay C.M., Caraty A., and Clarke I.J. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 148 (2006) 1150-1157
53. Smith J.T., Dungan H.M., Stoll E.A., Gottsch M.L., Braun R.E., Eacker S.M., Clifton D.K., and Steiner R.A. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146 (2005) 2976-2984
54. Sokal R.R., and Rohlf F.J. Biometry. The Principles and Practice of Statistics in Biological Research. 2nd ed. (1981), W.H. Freeman, NY pp. 859
55. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
56. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
57. Thompson E.L., Patterson M., Murphy K.G., Smith K.L., Dhillo W.S., Todd J.F., Ghatei M.A., and Bloom S.R. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J. Neuroendocrinol. 16 (2004) 850-858
58. Tsutsui K., Bentley G.E., Ubuka T., Saigoh E., Yin H., Osugi T., Inoue K., Chowdhury V.S., Ukena K., Ciccone N., Sharp P.J., and Wingfield J.C. The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). Gen. Comp. Endocrinol. 153 (2007) 365-370
59. van Aerle R., Kille P., Lange A., and Tyler C.R. Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish. Peptides 29 (2008) 57-64
60. Weltzien F.A., Andersson E., Andersen Ø., Shalchian-Tabrizi K., and Norberg B. The brain-pituitary-gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp. Biochem. Physiology. A 137 (2004) 447-477
61. Yu W.H., Karanth S., Walczewska A., Sower S.A., and McCann S.M. A hypothalamic follicle-stimulating hormone-releasing decapeptide in the rat. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 9499-9503