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

General and Comparative Endocrinology

Volumn 169, Issue 1, 2010, Pages 28-38

  Selvaraj, Sethu ^a   Kitano, Hajime ^a   Fujinaga, Yoichiro ^a   Ohga, Hirofumi ^a   Yoneda, Michio ^b   Yamaguchi, Akihiko ^a   Shimizu, Akio ^b   Matsuyama, Michiya ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b FISHERIES RESEARCH AGENCY   (Japan)

Author keywords

Brain; Gonadal stages; Gonads; Kiss1; Kiss2; Kisspeptins; Mackerel; Pituitary

Indexed keywords

COMPLEMENTARY DNA; KISSPEPTIN; KISSPEPTIN 1; KISSPEPTIN 10; KISSPEPTIN 2; MESSENGER RNA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; FEMALE; FISH; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOME SIZE; GONAD; GONAD DEVELOPMENT; HYPOPHYSIS; MACKEREL; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEX DIFFERENCE; SPAWNING; SPERMATOGENESIS; TISSUE DISTRIBUTION; VITELLOGENESIS;

EID: 77956611314     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2010.07.011     Document Type: Article

References (58)

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. Bilban M., Ghaffari-Tabrizi N., Hintermann E., Bauer S., Molzer S., Zoratti C. Kisspeptin-10, a Kiss-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J. Cell Sci. 2004, 117:1319-1328.
3. 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.
4. Brown R.E., Imran S.A., Ur E., Wilkinson M. KiSS-1 mRNA in adipose tissue is regulated by sex hormones and food intake. Mol. Cell. Endocrinol. 2008, 281:64-72.
5. Bustin S., Benes V., Garson J., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M., Shipley G., Vandesompele J., Wittwer C. The MIQE guidelines: minimal information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
6. Castellano J.M., Gaytan M., Roa J., Vigo E., Navarro V.M., Bellido C. Expression of KiSS-1 in rat ovary: putative local regulator of ovulation. Endocrinology 2006, 147:4852-4862.
7. Collette B.B. Family Scombridae Rafinesque 1815 - mackerels, tunas and bonitos. In: Annotated Checklists of Fishes, No. 19 2003, California Academy of Sciences, San Francisco.
8. d'Anglemont de Tassigny X., Fagg L.A., Dixon J.P., Day K., Leitch H.G., Hendrick A.G., Zahn D., Franceschini I., Caraty A., Carlton M.B., Aparicio S.A., Colledge W.H. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc. Natl. Acad. Sci. USA 2007, 104:10714-10719.
9. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., 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.
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., Bloom S.R. Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J. Clin. Endocrinol. Metab. 2005, 90:6609-6615.
11. 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.
12. Filby A.L., van Aerle R., Duitman J.W., Tyler C.R. The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol. Reprod. 2008, 78:278-289.
13. Funes S., Hedrick J.A., Vassileva G., Markowitz L., Abbondanzo S., Golovko A., Yang S., 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.
14. Gaytán F., Gaytán M., Castellano J.M., Romero M., Roa J., Aparicio B., Garrido N., Sánchez-Criado J.E., Millar R.P., Pellicer A., Fraser H.M., Tena-Sempere M. KiSS-1 in the mammalian ovary: distribution of kisspeptin in human and marmoset and alterations in KiSS-1 mRNA levels in a rat model of ovulatory dysfunction. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E520-E531.
15. Guilgur L.G., Ortí G., Strobl-Mazzulla P.H., Fernandino J.I., Miranda L.A., Somoza G. Characterization of the cDNAs encoding three GnRH forms in the pejerrey fish Odontesthesbonariensis (Atheriniformes) and the evolution of GnRH precursors. J. Mol. Evol. 2007, 64:614-627.
16. Gutiérrez-Pascual E., Martínez-Fuentes A.J., Pinilla L., Tena-Sempere M., Malagón M.M., Castaño J.P. Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs, and stimulation of luteinizing hormone and growth hormone secretion. J. Neuroendocrinol. 2007, 19:521-530.
17. 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.
18. Gottsch M.L., Clifton D.K., Steiner R.A. From KISS1 to kisspeptins: an historical perspective and suggested nomenclature. Peptides 2009, 30:4-9.
19. Harmin S.A., Crim L.W., Wiegand M.D. Plasma sex steroid profiles and the seasonal reproductive cycle in male and female winter flounder, Pleuronectes americanus. Mar. Biol. 1995, 121:601-610.
20. Hwang S.D., Lee T.W. Spawning dates and early growth of chub mackerel Scomber japonicus as indicated by otolith microstructure of juveniles in the inshore nursery ground. Fish. Sci. 2005, 71:1185-1187.
21. Irwig M.S., Fraley G.S., Smith J.T., Acohido B.V., Popa S.M., Cunningham M.J., Gottsch M.L., Clifton D.K., Steiner R.A. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004, 80:264-272.
22. Kadokawa H., Matsui M., Hayashi K., Matsunaga N., Kawashima C., Shimizu T., Kida K., Miyamoto A. Peripheral administration of kisspeptin-10 increases plasma concentrations of GH as well as LH in prepubertal Holstein heifers. J. Endocrinol. 2008, 196:331-334.
23. 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.
24. Kauffman A.S., Clifton D.K., Steiner R.A. Emerging ideas about kisspeptin-GPR54 signaling in the neuroendocrine regulation of reproduction. Trends Neurosci. 2007, 30:504-511.
25. Kime D.E. Classical and nonclassical reproductive steroids in fish. Rev. Fish Biol. Fish 1993, 3:160-180.
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., Vandenbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., Brezillon S., Tyldesley R., Suarez-Huerta N., Vandeput F. 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. Lapatto R., Pallais J.C., Zhang D., Chan Y.M., Mahan A., Cerrato F., Le W.W., Hoffman G.E., Seminara S.B. Kiss1-/-mice exhibit more variable hypogonadism than Gpr54-/-mice. Endocrinology 2007, 148:4927-4936.
29. Larionov A., Krause A., Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 2005, 6:62.
30. 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.
31. Lee J.H., Welch D.R. Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1. Cancer Res. 1997, 57:2384-2387.
32. Li S., Zhang Y., Liu Y., Huang X., Huang W., Lu D., Zhu P., Shi Y., Cheng C.H.K., Liu X., Lin H. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J. Endocrinol. 2009, 201:407-418.
33. Matsuyama M., Shiraishi T., Sundaray J.K., Rahman M.A., Ohta K., Yamaguchi A. Steroidogenesis in ovarian follicles of chub mackerel, Scomber japonicus. Zool. Sci. 2005, 22:101-110.
34. Mendiola D., Yamashita Y., Matsuyama M., Alvarez P., Tanaka M. Scomber japonicus, H. is a better candidate species for juvenile production activities than Scomber scombrus, L. Aqua. Res. 2008, 39:1122-1127.
35. 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.
36. Muir A.I., Chamberlain L., Elshourbagy N.A., Michalovich D., Moore D.J., Calamari A., Szekeres P.G., Sarau H.M., Chambers J.K., Murdock P. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J. Biol. Chem. 2001, 276:28969-28975.
37. Murphy K.G. Kisspeptins: regulators of metastasis and the hypothalamic-pituitary-gonadal axis. J. Neuroendocrinol. 2005, 17:519-525.
38. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Barreiro M.L., Casanueva F.F., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005, 146:1689-1697.
39. Nocillado J.N., 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 gray mullet, Mugil cephalous. Gen. Comp. Endocrinol. 2007, 150:278-287.
40. Ohta K., Mine T., Yamaguchi A., Matsuyama M. Sexually dimorphic expression of pituitary glycoprotein hormones in a sex-changing fish (Pseudolabrus sieboldi). J. Exp. Zool. 2008, 309A:534-541.
41. 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., Ususki 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.
42. Richard N., Galmiche G., Corvaisier S., Caraty A., Kottler M.L. KiSS-1 and GPR54 genes are co-expressed in rat gonadotrophs and differentially regulated in vivo by oestradiol and gonadotrophin-releasing hormone. J. Neuroendocrinol. 2008, 20:381-393.
43. Roa J., Vigo E., Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Casanueva F.F., 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.
44. 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.
45. Roa J., Tena-Sempere M. KiSS-1 system and reproduction: comparative aspects and roles in the control of female gonadotropic axis in mammals. Gen. Comp. Endocrinol. 2007, 153:132-140.
46. Roseweir A.K., Millar R.P. The role of kisspeptin in the control of gonadotrophin secretion. Hum. Reprod. Update 2009, 15:203-212.
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. The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 2003, 349:1614-1627.
48. 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. USA 2005, 102:2129-2134.
49. Sherwood N., Wu G.C.E. Developmental role of GnRH and PACAP in a zebrafish model. Gen. Comp. Endocrinol. 2005, 142:74-80.
50. Shiraishi T., Ohta K., Yamaguchi A., Yoda M., Chuda H., Matsuyama M. Reproductive parameters of the chub mackerel Scomber japonicus estimated from human chorionic gonadotropin induced final oocyte maturation and ovulation in captivity. Fish. Sci. 2005, 71:531-542.
51. Shiraishi T., Okamoto K., Yoneda M., Sakai T., Ohshimo S., Onoe S., Yamaguchi A., Matsuyama M. Age validation, growth and annual reproductive cycle of chub Scomber japonicus off the waters of northern Kyushu and in the East China Sea. Fish. Sci. 2008, 74:947-954.
52. Smith J.T. Kisspeptin signaling in the brain: steroid regulation in the rodent and ewe. Brain Res. Rev. 2008, 57:288-298.
53. 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.
54. Tena-Sempere M. Kisspeptin signaling in the brain: recent developments and future challenges. Mol. Cell. Endocrinol. 2010, 314:164-169.
55. Tena-Sempere M. Roles of kisspeptins in the control of hypothalamic-gonadotropic function: focus on sexual differentiation and puberty onset. Endocr. Dev. 2010, 17:52-62.
56. 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.
57. Yang B., Jiang Q., Chan T., Ko K.W.W., Wong A.O.L. 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.
58. Zohar Y., Muñoz-Cueto J.A., Elizur A., Kah O. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 2010, 165:438-455.