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Effects of Fasting on Brain Expression of Kiss2 and GnRH I and Plasma Levels of Sex Steroid Hormones, in Nile Tilapia Oreochromis niloticus

절식이 나일 틸라피아 Oreochromis niloticus의 Kiss2, GnRH I mRNA 발현 및 성 스테로이드 호르몬 농도에 미치는 영향

  • Park, Jin Woo (Marine Ecosystem and Biological Research Center, KIOST) ;
  • Kwon, Joon Yeong (Department of Aquatic Life Medical Sciences, College of Health Science, Sunmoon University) ;
  • Jin, Ye Hwa (Department of Aquatic Life Medical Sciences, College of Health Science, Sunmoon University) ;
  • Oh, Sung-Yong (Tongyeong Marine Science Station, KIOST)
  • 박진우 (한국해양과학기술원 생태기반연구센터) ;
  • 권준영 (선문대학교 건강보건대학 수산생명의학과) ;
  • 진예화 (선문대학교 건강보건대학 수산생명의학과) ;
  • 오승용 (한국해양과학기술원 통영해상과학기지)
  • Received : 2015.09.07
  • Accepted : 2016.02.25
  • Published : 2016.03.30

Abstract

In many fish species, including Nile tilapia (Oreochromis niloticus), gonadal development occurs at the expense of stored energy and nutrients. Therefore, reproductive systems are inhibited by limited food supply. It has been well established that reproductive function is highly sensitive to both metabolic status and energy balance. Nothing is known about the possible mediated connection between energy balance and reproduction. Kisspeptin, a neuropeptide product of the Kiss gene has emerged as an essential gatekeeper of reproduction and may be possibly be linked to energy balance and reproduction in non-mammalians. Thus, in this study, the effect of fasting (10 days) on the expression of kisspeptin and the gonadotropin-releasing hormone (GnRH) gene were assessed in Nile tilapia (male and female) using qRT-PCR. In addition, plasma levels of estradiol-$17{\beta}$ ($E_2$) and 11-ketotestosterone (11-KT) in adult tilapia were measured by ELISA. In male tilapia, fasting reduced Kiss2 and GnRH I mRNA expression in the brain and 11-KT level in comparison with the fed tilapia (p < 0.05). In females, however, there were no significant differences in GnRH I mRNA expression and $E_2$ between fish subjected to fasting and those fed (p > 0.05). These data indicate the impact of nutritional states on kisspeptin as a potential regulatory mechanism for the control of reproduction in male Nile tilapia.

Keywords

References

  1. Biran J, Ben-Dor S, Levavi-Sivan B (2008) Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol Reprod 79:776-786 https://doi.org/10.1095/biolreprod.107.066266
  2. Bronson FH (1986) Food-restricted, prepubertal, female rats: rapid recovery of luteinizing hormone pulsing with excess food, and full recovery of pubertal development with gonadotropin-releasing hormone. Endocrinology 118:2483-2487 https://doi.org/10.1210/endo-118-6-2483
  3. Brown RE, Imran SA, Ur E, Wilkinson M (2008) KiSS-1 mRNA in adipose tissue is regulated by sex hormones and food intake. Mol Cell Endocrinol 281:64-72 https://doi.org/10.1016/j.mce.2007.10.011
  4. Burcelin R, Thorens B, Glauser M, Gaillard RC, Pralong FP (2003) Gonadotropin-releasing hormone secretion from hypothalamic neurones: stimulation by insulin and potentiation by leptin. Endocrinology 144:4484-4491 https://doi.org/10.1210/en.2003-0457
  5. Cagampang FR, Maeda KI, Tsukamura H, Ohkura S, Ota K (1991) Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats. J Endocrinol 129: 321-328 https://doi.org/10.1677/joe.0.1290321
  6. Castellano JM, Navarro VM, Fernandez-Fernandez R, Nogueiras R, Tovar S, Roa J, Vazquez MJ, Vigo E, Casanueva FF, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M (2005) Change in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 146: 3917-3925 https://doi.org/10.1210/en.2005-0337
  7. Cowley MA (2003) Hypothalamic melanocortin neurons integrate signals of energy state. Eur J Pharmacol 480:3-11 https://doi.org/10.1016/j.ejphar.2003.08.087
  8. Dhillo WS, Murphy KG, Bloom SR (2007) The neuroendocrine physiology of kisspeptin in the human. Rev Endocr Metab Dis 8:41-46 https://doi.org/10.1007/s11154-007-9029-1
  9. Felip A, Zanuy S, Pineda R, Pinilla L, Carrillo M, Tena- Sempere M, Gomez A (2009) 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 312:61-71 https://doi.org/10.1016/j.mce.2008.11.017
  10. Filby AL, van Aerle R, Duitman J, Tyler CR (2008) The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol Reprod 78:278-289 https://doi.org/10.1095/biolreprod.107.063420
  11. Forbes S, Li XF, Kinsey-Jones J, O'Byrne K (2009) Effects of ghrelin on kisspeptin mRNA expression in the hypothalamic medial preoptic area and pulsatile luteinizing hormone secretion in the female rat. Neurosci Lett 460: 143-147 https://doi.org/10.1016/j.neulet.2009.05.060
  12. Foster DL, Ebling FJ, Micka AF, Vannerson LA, Bucholtz DC, Wood RI (1989) Metabolic interfaces between growth and reproduction. I. Nutritional modulation of gonadotropin, prolactin, and growth hormone secretion in the growth-limited female lamb. Endocrinology 125:342- 50 https://doi.org/10.1210/endo-125-1-342
  13. Grone BP, Carpenter RE, Lee M, Maruska KP, Fernald RD (2012) Food deprivation explains effects of mouthbrooding on ovaries and steroid hormones, but not brain neuropeptide and receptor mRNAs, in an African cichlid fish. Horm Behav 62:18-26 https://doi.org/10.1016/j.yhbeh.2012.04.012
  14. Gruenewald DA, Matsumoto AM (1993) Reduced gonadotropinreleasing hormone gene expression with fasting in male rat brain. Endocrinology 132:480-482 https://doi.org/10.1210/endo.132.1.8419144
  15. Horvath TL, Castaneda T, Tang-Christensen M, Pagotto U, Tschop MH (2003) Ghrelin as a potential anti-obesity target. Curr Pharm Design 9:1383-1395 https://doi.org/10.2174/1381612033454748
  16. Hoskins LJ, Xu M, Volkoff H (2008) Interactions between gonadotropin-releasing hormone (GnRH) and orexin in the regulation of feeding and reproduction in goldfish (Carassius auratus). Horm Behav 54:379-385 https://doi.org/10.1016/j.yhbeh.2008.04.011
  17. Iwasa T, Matsuzaki T, Murakami M, Kinouchi R, Gereltsetseg G, Fujisawa S, Kuwahara A, Yasui T, Irahara M (2010) Sensitivities of mRNA expression levels of Kiss1 and its receptor, Kiss1r, to nutritional status are changed during the developmental period in female rats. J Endocrinol 207:195-202 https://doi.org/10.1677/JOE-10-0129
  18. Kaiya H, Kojima M, Hosoda H, Moriyama S, Takahashi A, Kawauchi H, Kangawa K (2003a) Peptide purification, complementary deoxyribonucleic acid (DNA) and genomic DNA cloning, and functional characterization of ghrelin in rainbow trout. Endocrinology 144:5215-5226 https://doi.org/10.1210/en.2003-1085
  19. Kaiya H, Kojima M, Hosoda H, Riley LG, Hirano T, Grau EG, Kangawa K (2003b) Amidated fish ghrelin: purification, cDNA cloning in the Japanese eel and its biological activity. J Endocrinol 176:415-423 https://doi.org/10.1677/joe.0.1760415
  20. Kitahashi T, Ogawa S, Parhar IS (2009) Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150:821-831 https://doi.org/10.1210/en.2008-0940
  21. Kohsaka A, Watanobe H, Kakizaki Y, Suda T, Schioth HB (2001) A significant participation of orexin-A, a potent orexigenic peptide, in the preovulatory luteinizing hormone and prolactin surge in the rat. Brain Res 898:166-170 https://doi.org/10.1016/S0006-8993(01)02157-6
  22. Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, Welch DR (1996) KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer I 88:1731-1737 https://doi.org/10.1093/jnci/88.23.1731
  23. Lee YR, Tsunekawa K, Moon MJ, Um HN, Hwang JI, Osugi T, Otaki MN, Sunakawa Y, Kim K, Vaudry H, Kwon HB, Seong JY (2009) Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150:2837-2846 https://doi.org/10.1210/en.2008-1679
  24. Li S, Zhang Y, Liu Y, Huang X, Huang W, Lu D, Zhu P, Shi Y, Cheng CHK, Liu X, Lin H (2009) Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J Endocrinol 201:407-418 https://doi.org/10.1677/JOE-09-0016
  25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408 https://doi.org/10.1006/meth.2001.1262
  26. Luque RM, Kineman RD, Tena-Sempere M (2007) Regulation of hypothalamic expression of KiSS-1 and GPR54 genes by metabolic factors: analyses using models and a cell line. Endocrinology 148:4601-4611 https://doi.org/10.1210/en.2007-0500
  27. Mechaly AS, Vinas J, Piferrer F (2011) 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. Mol Cell Endocrinol 339:14-24 https://doi.org/10.1016/j.mce.2011.03.004
  28. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA (2005) Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. P Natl Acad Sci USA 102:1761-1766 https://doi.org/10.1073/pnas.0409330102
  29. Mircea CN, Lujan ME, Pierson RA (2007) Metabolic fuel and clinical implications for female reproduction. J Obstet Gynaecol Can 29:887-902 https://doi.org/10.1016/S1701-2163(16)32661-5
  30. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S (2001) A role for ghrelin in the central regulation of feeding. Nature 409:194-198 https://doi.org/10.1038/35051587
  31. Nishiguchi R, Azuma M, Yokobori E, Uchiyama M, Matsuda K (2012) Gonadotropin-releasing hormone 2 suppresses food intake in the zebrafish, Danio rerio. Front Endocrinol 3:122
  32. Parhar IS, Ogawa S, Sakuma Y (2004) 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 145:3613-3618 https://doi.org/10.1210/en.2004-0395
  33. Parhar IS, Sato H, Sakuma Y (2003) Ghrelin gene in cichlid fish is modulated by sex and development. Biochem Bioph Res Co 305:169-175 https://doi.org/10.1016/S0006-291X(03)00729-0
  34. Patterson M, Murphy KG, Thompson EL, Patel S, Ghatei MA, Bloom SR (2006) Administration of kisspeptin-54 into discrete regions of the hypothalamus potently increases plasma luteinising hormone and testosterone in male adult rats. J Neuroendocrinol 18:349-354 https://doi.org/10.1111/j.1365-2826.2006.01420.x
  35. Popa SM, Clifton DK, Steiner RA (2008) The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction. Annu Rev Physiol 70:213-238 https://doi.org/10.1146/annurev.physiol.70.113006.100540
  36. Roa J, Tena-Sempere M (2007) KiSS-1 system and reproduction: comparative aspects and roles in the control of female gonadotropic axis in mammals. Gen Comp Endocr 153:132-140 https://doi.org/10.1016/j.ygcen.2007.01.026
  37. Sakata I, Nakamura K, Yamazaki M, Matsubara M, Hayashi Y, Kangawa K, Sakai T (2002) Ghrelin-producing cells exist as two types of cells, closed- and opened-type cells, in the rat gastrointestinal tract. Peptides 23:531-536 https://doi.org/10.1016/S0196-9781(01)00633-7
  38. Schneider JE (2004) Energy balance and reproduction. Physiol Behav 81:289-317 https://doi.org/10.1016/j.physbeh.2004.02.007
  39. Sisk CL, Bronson FH (1986) Effects of food restriction and restoration on gonadotropin and growth hormone secretion in immature male rats. Biol Reprod 35:554-561 https://doi.org/10.1095/biolreprod35.3.554
  40. Smith C, Wootton RJ (1994) The cost of parental care in Haplochromis argens (Cichlidae). Environ Biol Fish 40:99-104 https://doi.org/10.1007/BF00002184
  41. Smith C, Wootton RJ (1995) The costs of parental care in teleost fishes. Rev Fish Biol Fisher 5:7-22 https://doi.org/10.1007/BF01103363
  42. Tacon P (1996) Relationships between the expression of maternal behaviour and ovarian development in the mouthbrooding cichlid fish Oreochromis niloticus. Aquaculture 146:261-275 https://doi.org/10.1016/S0044-8486(96)01389-0
  43. Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien F-A, Dufour S, Karlsen O, Norberg B, Andersson E, Hansen T (2010) Control of puberty in farmed fish. Gen Comp Endocr 165:483-515 https://doi.org/10.1016/j.ygcen.2009.05.004
  44. Tuziak SM, Volkoff H (2013) Gonadotrophin-releasing hormone in winter flounder (Pseudopleuronectes americanus): molecular characterization, distribution and effects of fasting. Gen Comp Endocr 184:9-21 https://doi.org/10.1016/j.ygcen.2012.12.010
  45. Unniappan S, Lin X, Cervini L, Rivier J, Kaiya H, Kangawa K, Peter RE (2002) Goldfish ghrelin: molecular characterization of the complementary deoxyribonucleic acid, partial gene structure and evidence for its stimulatory role in food intake. Endocrinology 143:4143-4146 https://doi.org/10.1210/en.2002-220644
  46. Volkoff H, Canosa LF, Unniappan S, Cerda-Reverter JM, Bernier NJ, Kelly SP, Peter RE (2005) Neuropeptides and the control of food intake in fish. Gen Comp Endocr 142:3-19 https://doi.org/10.1016/j.ygcen.2004.11.001
  47. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA, Batterham RL, Taheri S, Stanley SA, Ghatei MA, Bloom SR (2001) Ghrelin causes hyperphagia and obesity in rats. Diabetes 50:2540-2547 https://doi.org/10.2337/diabetes.50.11.2540