Determination of Rutilus kutum kisspeptin and its effect on reproductive hormones

Document Type : Research Paper

Authors

1 Ph.D. Student in Biochemistry, Faculty of Sciences, University of Guilan, Rasht, Iran

2 Associate Professor in Department of Biology, Faculty of Sciences, University of Guilan, Rasht, Iran

3 Associate Professor in Department of Biochemistry and Biophysics, Institute of Biochemistry and Biophysics, University of Tehran, Tehran, Iran

4 Professor in Department of Biology, Faculty of Sciences, University of Guilan, Rasht, Iran

5 Associate Professor in Department of Marine Sciences, Caspian Sea Basin Research Center, University of Guilan, Rasht, Iran

6 Professor in Department of Medicinal Chemistry, Institute of Synthesis Chemistry, K.N. Toosi University of Technology, Tehran, Iran

Abstract

The Caspian kutum (Rutilus kutum) is the most important commercially and nutritionally bony fish, which is used to prevent the extinction of this valuable species by induced reproduction to synchronize and increase the level of fecundity in breeding conditions. Previous research has shown that kisspeptin, a super-stimulatory protein in the sex-secreting gland axis, leads to puberty and gametogenesis. However, the sequence of kisspeptin 1 and 2 of R. kutum has not been determined and the ability of this peptide from protein (Kiss1) in reproduction has not been studied so far. In the present study, the kisspeptin10 sequence of R. kutum was determined by CLUSTALW method by designing a primer from the Kiss1 sequence of the same family fish of R. kutum. Doses of 5, 25, 50 and 100μg/kg were used to achieve the best dose of this peptide; and concentrations of 17-α hydroxy progesterone and 17-β estradiol were examined. The results of this study showed that synthetic kisspeptin 10 with an optimal dose of 100μg/kg can be introduce as a suitable candidate for induction of spawning in R. kutum.

Keywords


 Abdurakhmanov Y.A. 1962. Fish of freshwater bodies of Azerbaijan. Academy of Sciences of Azerbaijan SSR, USSR. P: 89–96.
Akhondian M., Savari A., Salamat N., Movahdynya A.A. and Salari M.A. 2015. Changes in plasma level of steroid hormones (estradiol 17β, 17α20β hydroxy progesteron and cortisol) and electrolytes, during different stages of reproductive cycle in Rutilus rutilus caspicus from Bandar Torkaman (South of Caspian Sea). Oceanography, 6(21): 117–126.
Al-Khalaifah H.S., Amer S.A., Al-Sadek D.M.M., Khalil A.A., Zaki E.M. and El-Araby D.A. 2020. Optimizing the growth, health, reproductive performance, and gonadal histology of broodstock fantail goldfish (Carassius auratus, L.) by dietary cacao bean meal. Animals (Basel), 10(10): 1–22 (1808).
Apter D., Butzow T.L., Laughlin G.A. and Yen S.S. 1993. Gonadotropin- releasing hormone pulse generator activity during pubertal transition in girls: Pulsatile and diurnal patterns of circulating gonadotropins. The Journal of Clinical Endocrinology and Metabolism, 76: 940–949.
Asimakopoulos B. 2012. Hypothalamus-pituitary-gonadal axis: It is time for revision. Human Genetics and Embryology, 2: 1–3.
Clarke I.J. and Cummins J.T. 1982. The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. Endocrinology, 111: 1737–1739.
Coad B.W. and Vilenkin B.Y. 2004. Co-occurrence and zoogeography of the freshwater fishes of Iran. Zoology in the Middle East, 31: 53–61.
Corradi P.F., Corradi R.B. and Greene L.W. 2016. Physiology of the hypothalamic pituitary gonadal axis in the male. Urologic Clinics of North America, 43: 151–162.
De Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L. and Milgrom E. 2003. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proceedings of the National Academy of Sciences of the United States of America, 100: 10972–10976.
Faheem M., Jahan N., Khaliq S. and Lone K.P. 2019. Modulation of brain kisspeptin expression after bisphenol-A exposure in a teleost fish, Catla catla. Fish Physiology and Biochemistry, 45(1): 33–42.
Freeman M.E. 1994. The neuroendocrine control of the ovarian cycle of the rat. P: 613–658. In: Knobil E. and Neill J.D. (Eds.). The Physiology of Reproduction. Raven Press Ltd, USA.
Goodman R.L. 1994. Neuroendocrine control of the ovine estrous cycle. P: 659–710. In: Knobil E., Neill J.D. (Eds.). The Physiology of Reproduction. Raven Press Ltd, USA.
Goodman R.L. and Inskeep E.K. 2006. Neuroendocrine control of the ovarian cycle of the sheep. 2247–2389. In: Neill J.D. (Ed.). Physiology of Reproduction. Academic Press, USA.
Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., Seminara S., Clifton D.K. and Steiner R.A. 2004. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology, 145(9): 4073–4077.
Haniffa M.A., Merlin T. and Shaik Mohamed J. 2000. Induced spawning of the striped murrel Channa striatus using pituitary extracts, human chorionic gonadotropon, luteinizing hormone releasing hormone analogue, and ovaprim. Acta Icthyologica et Piscatorial, 30(1): 53–60.
Heyrati F.P., Mostafavi H., Toloee H. and Dorafshan S. 2006. Induced spawning of kutum, Rutilus frisii kutum using (D-Ala6, Pro9-NEt) GnRHa combined with domperidone. Aquaculture, 265: 288–293.
Kiabi B.H., Abdoli A. and Naderi M. 1999. Status of fish fauna in the south Caspian basin of Iran. Zoology in the Middle East, 18: 57–65.
Kotani M., Detheux M., Van Den Bogaerde A., Communi D., Van Der Winden J.M., Le P.E., Brezillon S., Tyldesley R., Suarez-Huerta N., Vandeput F., Blanpain C., Schiffmann S.N., Vassart G. and Parmentier M. 2001. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. Journal of Biological Chemistry, 276(37): 34631–34636.
Lee J.H., Miele M.E., Hicks D.J., Phillips K.K., Trent J.M., Weissman B.E. and Welch D.R. 1996. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. Journal of the National Cancer Institute, 88 (23): 1731–1737.
Lee D.K., Nguyen T., O'Neill G.P., Cheng R., Liu Y., Howard A.D., Coulombe N., Tan C.P., Tang-Nguyen A.T., George S.R. and O'Dowd B.F. 1999. Discovery of a receptor related to the galanin receptors. Federation of European Biochemical Societies letters, 446(1): 103–107.
Lee P.Y., Costumbrado J., Hsu C.Y. and Kim Y.H. 2012. Agarose gel electrophoresis for the separation of DNA fragments. Journal of Visualized Experiments, 62: 1–5 (3923).
Li S., Zhang Y., Liu Y., Huang X., Huang W., Lu D., Zhu P., Shi Y., Cheng C.H. and Liu X. 2009. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). Journal of Endocrinology, 201: 407–418.
Lorenz T.C. 2012. Polymerase chain reaction: Basic protocol plus troubleshooting and optimization strategies. Journal of Visualized Experiments, 63: 1–15 (e3998).
Mitani Y., Kanda S., Akazome Y., Zempo B. and Oka Y. 2010. Hypothalamic Kiss1 but not Kiss2 neurons are involved in estrogen feedback in medaka (Oryzia slatipes). Endocrinology, 151(4): 1751–1759.
  Moles G., Gomez A., Carrillo M. and Zanuy S. 2012. Development of a homologous enzyme linked immunosorbent assay for European sea bass FSH. Reproductive cycle plasma levels in both sexes and in yearling precocious and non-precocious males. General and Comparative Endocrinology, 176(1): 70–78.
 Moles G., Gomez A., Rocha A., Carrillo M. and Zanuy S. 2008. Purification and characterization of follicle-stimulating hormone from pituitary glands of sea bass (Dicentrarchus labrax). General and Comparative Endocrinology, 158: 68–76.
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., Steplewski K., Shabon U., Miller J.E., Middleton S.E., Darker J.G., Larminie C.G.C., Wilson S., Bergsma D.J., Emson P., Faull R., Philpott K.L. and Harrison D.C. 2001. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. Journal of Biological Chemistry, 276: 28969–28975.
Mylonas C.C., Fostier A. and Zanuy S. 2010. Broodstock management and hormonal manipulations of  fish reproduction. General and Comparative Endocrinology, 165(3): 516–534.
Nash J.P., Cuisset-Davail B., Bhattacharyya S., Suter H.C., Menn F. and Kime D.E. 2000. An enzyme linked immunosorbent assay (ELISA) for testosterone, estradiol, and 17, 20- dihydroxy-4-pregnen-3-one using acetylcholinesterase as tracer: Application to measurement of diel patterns in rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry, 22: 355–363.
Niida A., Wang Z., Tomita K., Oishi S., Tamamura H., Otaka A., Navenot J.M., Broach J.R., Peiper S.C. and Fujii N. 2006. Design and synthesis of downsized metastin (45-54) analogs with maintenance of high KISS1RA agonistic activity. Bioorganic and Medicinal Chemistry Letters, 16(1): 134–137.
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. and Fujino M. 2001.  Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature, 411: 613–617.
Ojeda S.R., Lomniczi A., Mastronardi C., Heger S., Roth C. and Parent A.S. 2006. Minireview: the neuroendocrine regulation of puberty: Is the time ripe for a systems biology approach. Endocrinology, 147: 1166–1174.
Poortenaar C., Hooker S. and Sharp N. 2001. Assessment of yellowtail kingfish (Seriola lalandi lalandi) reproductive physiology, as a basis for aquaculture development. Aquaculture, 201: 271–286.
Rodriguez L., Begtashi I., Zanuy S. and Carrillo M. 2000. Development and validation of an enzyme immunoassay for testosterone: Effects of photoperiod on plasma testosterone levels and gonadal development in male sea bass (Dicentrarchus labrax, L.) at puberty. Fish Physiology and Biochemistry, 23: 141–150.
Rodriguez L., Begtashi I., Zanuy S., Shaw M. and Carrillo M. 2001. Changes in plasma levels of reproductive hormones during first sexual maturation in European male sea bass (Dicentrarchus labrax L.) under artificial day lengths. Aquaculture, 202: 235–248.
Saridhar S., Vijayakumar C. and Haniffa M.A. 1998. Induced spawning and establishment of captive population for an endangered fish, Ompok bimaculatus in India. Current Science, 75(10): 1066–1068.
Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno Jr 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., Crowley Jr W.F., Aparicio S.A. and Colledge W.H. 2003. The GPR54 gene as a regulator of puberty. The New England Journal of Medicine, 349: 1614–1627.
Sewald N. and Jakubke H.D. 2002. Peptides: Chemistry and Biology. Wiley-VCH, German. 594P.
Shahab M., Mastronardi C., Seminara S.B., Crowley W.F., Ojeda S.R. and Plant T.M. 2005. Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates. Proceedings of the National Academy of Sciences of the United States of America, 102(6): 2129–2134.
Simerly R.B. 1998. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behavioural Brain Research, 92: 195–203.
Walker J.J., Terry J.R., Tsaneva-Atanasova K., Armstrong S.P., McArdle C.A. and Lightman S.L. 2010. Encoding and decoding mechanisms of pulsatile hormone secretion. Journal of Neuroendocrinology, 22: 1226–1238.
Zhao Y., Lin M.C.A., Mock A., Yang M. and Wayne N.L. 2014. Kisspeptins modulate the biology of multiple populations of gonadotropin-releasing hormone neurons during embryogenesis and adulthood in zebrafish (Danio rerio). PLOS One 9(8): 1–11 (e104330).
Zonneveld N., Rustidja Viveen W.J.A.R. and Mudana W. 1988. Induced spawning and egg incubation of the Asian catfish, Clarias batrachus. Aquaculture, 74: 41–47.