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Tissue-Specific Sexual Dimorphism in the Expression of kisspeptin and its Receptors in Spotted Snakehead Channa punctatus


Affiliations
1 Department of Zoology, University of Delhi, Delhi 110 007, India
 

The present study paves the way for novel aspects of kisspeptin in the regulation of fish physiology, importantly, immunity and metabolic activities. The expression level of kisspeptin (kiss1) and its receptors (kiss1r, kiss2r) was observed in different regions of the brain, primary and secondary lymphoid organs, liver and gonads of male and female Channa punctatus, suggesting a wider role of kisspeptin in the regulation of fish physiology. Further, expression profile of kiss1, kiss1r and kiss2r revealed sexual dimorphism depending on tissues. Surprisingly, insignificant correlation was observed between the expression of kiss1 and its receptors.

Keywords

Channa punctatus, Kisspeptin Receptors, Sexual Dimorphism, Teleost.
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  • Lee, J. H., Miele, M. E., Hicks, D. J., Philips, K. K., Trent, J. M., Weissman, B. E. and Welch, D. R., KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J. Natl. Cancer Inst., 1996, 88, 1731–1737.
  • Lee, D. K. et al., Discovery of a receptor related to the galanin receptors. FEBS Lett., 1999, 446, 103–107.
  • 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, 2004, 145, 3613–3618.
  • Selvaraj, S., Kitano, H., Fujinaga, Y., Ohga, H. and Yoneda, 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.
  • Ohga, H., Fujinaga, Y., Selvaraj, S., Kitano, H., Nyuji, M., Yamaguchi, A. and Matsuyama, M., Identification, characterization, and expression profiles of two subtypes of kisspeptin receptors in a scombroid fish (chub mackerel). Gen. Comp. Endocrinol., 2013, 193, 130–140.
  • Fairgrieve, M. R., Shibata, Y., Smith, E. K., Hayman, E. S. and Luckenbach, J. A., Molecular characterization of the gonadal kisspeptin system: cloning, tissue distribution, gene expression analysis and localization in sablefish (Anoplopoma fimbria). Gen. Comp. Endocrinol., 2016, 225, 212–223.
  • Song, H., Wang, M., Wang, Z., Liu, J., Qi, J. and Zhang, Q., Characterization of kiss2 and kissr2 genes and the regulation of kisspeptin on the HPG axis in Cynoglossus semilaevis. Fish Physiol. Biochem., 2017, 43, 731–753.
  • Tena-Sempere, M., Felip, A., Gómez, A., Zanuy, S. and Carrillo, M., Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. Gen. Comp. Endocrinol., 2012, 175, 234–243.
  • Lee, Y. R. et al., Molecular evolution of multiple forms of kisspeptin and GPR54 receptors in vertebrates. Endocrinology, 2009, 150, 2837–2846.
  • de Roux, N., Genin, E., Carel, J., Matsuda, F., Chaussain, J. and 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.
  • Felip, A., Zanuy, S., Pineda, R., Pinilla, L., Carrillo, M., TenaSempere, M. and 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.
  • Song, H., He, Y., Ma, L., Zhou, X., Liu, X., Qi, J. and Zhang, Q., Characterisation of kisspeptin system genes in an ovoviviparous teleost: Sebastes schlegeli. Gen. Comp. Endocrinol., 2015, 214, 114–125.
  • Yang, Y., Gao, J., Yuan, C. Zhang, Y., Guan, Y. and Wang, Z., Molecular identification of Kiss/GPR54 and function analysis with mRNA expression profiles exposure to 17α-ethinylestradiol in rare minnow Gobiocypris rarus. Mol. Biol. Rep., 2016, 43, 737–749.
  • Basak, R., Roy, A. and Rai, U., Seasonality of reproduction in male spotted murrel Channa punctatus: correlation of environmental variables and plasma sex steroids with histological changes in testis. Fish Physiol. Biochem., 2016, 42, 1249–1258.
  • 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., 2008, 786, 776–786.
  • Loveland, J. L., Uy, N., Maruska, K. P., Carpenter, R. E. and Fernald, R. D., Social status differences regulate the serotonergic system of a cichlid fish, Astatotilapia burtoni. J. Exp. Biol., 2014, 217, 2680–2690.
  • Pradhan, A. and Olsson, P., Zebrafish sexual behaviour: role of sex steroid hormones and prostaglandins. Behav. Brain Funct., 2015, 11(23), 1–10.
  • Livak, K. J. and Schmittgen, T. D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC T method. Methods, 2001, 25, 402–408.
  • Li, S. et al., Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J. Endocrinol., 2008, 201, 407–418.
  • Yang, B., Jiang, Q., Chan, T., Ko, W. K. W. and 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. Gen. Comp. Endocrinol., 2010, 165, 60–71.
  • Pasquier, J., Lafont, A. G., Leprince, J., Vaudry, H., Rousseau, K. and Dufour, S., First evidence for a direct inhibitory effect of kisspeptins on LH expression in the eel, Anguilla anguilla. Gen. Comp. Endocrinol., 2011, 173, 216–225.
  • Imamura, S., Hur, S., Takeuchi, Y., Bouchekioua, S. and Takemura, A., Molecular cloning of kisspeptin receptor genes (gpr54-1 and gpr54-2) and their expression profiles in the brain of a tropical damselfish during different gonadal stages. Comp. Biochem. Physiol. A, 2017, 203, 9–16.
  • Servili, A. et al., Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology, 2011, 152, 1527–1540.
  • Escobar, S., Servili, A., Felip, A., Zanuy, S., Carrillo, M. and Kah, O., Characterization of the kisspeptin systems in the brain of the European sea bass (Dicentrarchus labrax): relationships with oestrogen receptors. Indian J. Sci. Technol., 2011, 4, 23–24.
  • Escobar, S. et al., Expression of kisspeptins and kiss receptors suggests a large range of functions for kisspeptin systems in the brain of the European sea bass. PLOS ONE, 2013, 8(7), e70177, 1–18.
  • Escobar, S., Felip, A., Gueguen, M., Zanuy, S., Carrillo, M., Kah, O. and Servili, A., Expression of kisspeptins in the brain and pituitary of the European sea bass (Dicentrarchus labrax). J. Comp. Neurol., 2013, 521, 933–948.
  • Mitani, Y., Kanda, S., Akazome, Y., Zempo, B. and Oka, Y., Hypothalamic Kiss1 but not Kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes). Neuroendocrinology, 2015, 151, 1751–1759.
  • Muñoz-Cueto, J. A., Sarasquete, C., Zohar, Y. and Kah, O., An Atlas of the Brain of the Gilthead Seabream (Sparus aurata). A Maryland Sea Grant Publication, College Park, Maryland, USA, 2001.
  • Messager, S. et al., Kisspeptin directly stimulates gonadotropinreleasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. USA, 2005, 102, 1761–1766.
  • Ogawa, S., Ng, K. W., Ramadasan, P. N., Nathan, F. M. and Parhar, I. S., Habenular Kiss1 neurons modulate the serotonergic system in the brain of zebrafish. Endocrinology, 2012, 153, 2398–2407.
  • Ogawa, S. and Parhar, I. S., Biological significance of kisspeptinkiss1 receptor signaling in the habenula of teleosts species. Front. Endocrinol., 2018, 9(222), 1–8.
  • Sloley, B. D., Cunjak, R. A., Power, G. and Down, R. G. H., The influence of sex and spawning on levels of tryptophan, serotonin and 5-hydroxyindoleacetic acid in the brains of wild brook trout, Salvelinus forttinalis. J. Fish Biol., 1986, 29, 663–669.
  • Sajwan, M. K., Kavarthapu, R., Cheni-Chery, S., Anbazhagan, R., Yaraguntappa, B. and Balasubramanian, S., Cloning and expression analysis of tyrosine hydroxylase and changes in catecholamine levels in brain during ontogeny and after sex steroid analogues exposure in the catfish, Clarias batrachus. Gen. Comp. Endocrinol., 2014, 197, 18–25.
  • Kanda, S. et al., Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology, 2008, 149, 2467–2476.
  • Bohórquez, M. O. T., Mechaly, A. S., Hughes, L. C., Campanella, D., Ortí, G., Canosa, L. F. and Somoza, G. M., Kisspeptin system in pejerrey fish (Odontenthes bonariensis): characterization and gene expression pattern during early developmental stages. Comp. Biochem. Physiol. A, 2017, 204, 146–156.
  • Martinez-Chavez, C. C., Minghetti, M. and Migaud, H., GPR54 and rGnRH I gene expression during the onset of puberty in Nile tilapia. Gen. Comp. Endocrinol., 2008, 156, 224–233.
  • Nocillado, J. N., Biran, J., Lee, Y. Y., Levavi-sivan, B., Mechaly, A. S., Zohar, Y. and Elizur, A., The Kiss2 receptor (Kiss2r) gene in southern bluefin tuna, Thunnus maccoyii and in yellowtail kingfish, Seriola lalandi – functional analysis and isolation of transcript variants. Mol. Cell. Endocrinol., 2012, 362, 211–220.
  • Filby, A. L. et al., The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol. Reprod., 2008, 78, 278–289.
  • Ohga, H. et al., mRNA levels of kisspeptins, kisspeptin receptors, and GnRH1 in the brain of chub mackerel during puberty. Comp. Biochem. Physiol. A, 2015, 179, 104–112.
  • Kitahashi, T., Ogawa, S. and Parhar, I. S., Cloning and expression of kiss2 in the zebrafish and medaka. Neuroendocrinology, 2009, 150, 821–831.
  • Li, S. et al., Structural and functional multiplicity of the kisspeptin/ GPR54 system in goldfish (Carassius auratus). J. Endocrinol., 2009, 201, 407–418.
  • Mechaly, A. S., Piferrer, F. and Vi, J., 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 nonmammalian species. Mol. Cell. Endocrinol., 2011, 339, 14–24.
  • Ohtaki, T. et al., Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature, 2001, 411, 613–617.
  • Kotani, M. et al., 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.
  • Funes, S. et al., The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem. Biophys. Res. Commun., 2003, 312, 1357–1363.
  • Castellano, J. M. et al., Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology, 2006, 147, 4852–4862.
  • Tariq, A. R. et al., Kiss1 and Kiss1 receptor expression in the rhesus monkey testis: a possible local regulator of testicular function. Cent. Eur. J. Biol., 2013, 8, 968–974.
  • Terao, Y., Kumano, S., Takatsu, Y., Hattori, M., Nishimura, A., Ohtaki, T. and Shintani, Y., Expression of KiSS-1, a metastasis suppressor gene, in trophoblast giant cells of the rat placenta. Biochim. Biophys. Acta, 2004, 1678, 102–110.
  • Hussain, M. A., Song, W. and Wolfe, A., There is kisspeptin and then there is kisspeptin. Trends Endocrinol. Metab., 2015, 26, 564-572.
  • Aydin, M., Oktar, S., Yonden, Z., Ozturk, O. H. and Yilmaz, B., Direct and indirect effects of kisspeptin on liver oxidant and antioxidant systems in young male rats. Cell Biochem. Funct., 2010, 28, 293–299.
  • Alvarado, M. V., Carrillo, M. and Felip, A., Expression of kisspeptins and their receptors, gnrh-1/gnrhr-II-1a and gonadotropin genes in the brain of adult male and female European sea bass during different gonadal stages. Gen. Comp. Endocrinol., 2013, 187, 104–116.
  • Shahjahan, M., Motohashi, E., Doi, H. and 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.
  • Maddison, J. E., Page, S. W. and Church, D. B., Small Animal Clinical Pharmacology, Elsevier, 2008.

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  • Tissue-Specific Sexual Dimorphism in the Expression of kisspeptin and its Receptors in Spotted Snakehead Channa punctatus

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Authors

Amrita Bakshi
Department of Zoology, University of Delhi, Delhi 110 007, India
Umesh Rai
Department of Zoology, University of Delhi, Delhi 110 007, India

Abstract


The present study paves the way for novel aspects of kisspeptin in the regulation of fish physiology, importantly, immunity and metabolic activities. The expression level of kisspeptin (kiss1) and its receptors (kiss1r, kiss2r) was observed in different regions of the brain, primary and secondary lymphoid organs, liver and gonads of male and female Channa punctatus, suggesting a wider role of kisspeptin in the regulation of fish physiology. Further, expression profile of kiss1, kiss1r and kiss2r revealed sexual dimorphism depending on tissues. Surprisingly, insignificant correlation was observed between the expression of kiss1 and its receptors.

Keywords


Channa punctatus, Kisspeptin Receptors, Sexual Dimorphism, Teleost.

References





DOI: https://doi.org/10.18520/cs%2Fv116%2Fi5%2F802-810