Skip to main content
Log in

Ontogenetic and tissue-specific expression of gonadotropin-inhibitory hormone (GnIH) and its receptors in Catla catla

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Gonadotropin-inhibitory hormone (GnIH) is an RFamide peptide, and its role in reproduction is well studied from fish to mammals, but very few reports are available about the function of GnIH during larval development. In this study, we examined the GnIH and GnIH receptors (GnIHRs) expression from embryogenesis to adult stage and tissue-specific expression in adult Catla catla using quantitative real-time (qRT) PCR. The qRT PCR analysis of GnIH mRNA during ontogenetic development showed the increasing trend from early developmental stages to the adult stage with the highest expression in 24 months fish. However, the expression of two GnIH receptors, GnIHR1 and GnIHR2 also increased from larval stages to the adults with a peak at 17 days post-hatching, while GnIHR3 showed the higher mRNA expression during embryogenesis and then decreasing gradually. Tissue distribution analysis of GnIH showed the highest mRNA expression of GnIH in the brain, followed by gonads of both the sexes. GnIHR1 and GnIHR2 were also highly expressed in the brain and gonads of both the sexes, while GnIHR3 showed the highest expression in gonads of both the sexes without any expression in the brain. These results suggest that the brain is the primary site of action for GnIH, GnIHR1 and GnIHR2, while gonads for GnIHR3.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Aliaga-Guerrero M, Paullada-Salmerón JA, Piquer V, Mañanós EL, Muñoz-Cueto JA (2018) Gonadotropin-inhibitory hormone in the flatfish, Solea senegalensis: molecular cloning, brain localization and physiological effects. J Comp Neurol 526(2):349–370

    CAS  PubMed  Google Scholar 

  2. Bentley GE, Perfito N, Ukena K, Tsutsui K, Wingfield JC (2003) Gonadotropin-inhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone. J Neuroendocrinol 15(8):794–802

    CAS  PubMed  Google Scholar 

  3. Bentley GE, Ubuka T, McGuire NL, Chowdhury VS, Morita Y, Yano T, Hasunuma I, Binns M, Wingfield JC, Tsutsui K (2008) Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen Comp Endocrinol 156(1):34–43

    CAS  PubMed  Google Scholar 

  4. Biran J, Golan M, Mizrahi N, Ogawa S, Parhar IS, Levavi-Sivan B (2014) LPXRFa, the piscine ortholog of GnIH, and LPXRF receptor positively regulate gonadotropin secretion in tilapia (Oreochromis niloticus). Endocrinology. https://doi.org/10.1210/en.2013-2047

    PubMed  Google Scholar 

  5. Biswas S, Jadhao AG, Pinelli C, Palande NV, Tsutsui K (2015) GnIH and GnRH expressions in the central nervous system and pituitary of Indian major carp, Labeo rohita during ontogeny: an immunocytochemical study. Gen Comp Endocrinol 220:88–92

    CAS  PubMed  Google Scholar 

  6. Choi YJ, Habibi HR, Kil GS, Jung MM, Choi CY (2016) Effect of cortisol on gonadotropin inhibitory hormone (GnIH) in the cinnamon clownfish, Amphiprion melanopus. Biochem Biophys Res Commun 485:342–348

    Google Scholar 

  7. Corchuelo S, Martinez ER, Butzge AJ, Doretto LB, Ricci JM, Valentin FN, Nakaghi LS, Somoza GM, Nóbrega RH (2017) Characterization of Gnrh/Gnih elements in the olfacto-retinal system and ovary during zebrafish ovarian maturation. Mol Cell Endocrinol 15(450):1–3

    Google Scholar 

  8. Dardente H, Birnie M, Lincoln GA, Hazlerigg DG (2008) RFamide-related peptide and its cognate receptor in the sheep: cDNA cloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol 20(11):1252–1259

    CAS  PubMed  Google Scholar 

  9. Di Yorio MP, Muñoz-Cueto JA, Salmerón JA, Somoza GM, Tsutsui K, Vissio PG (2019) The gonadotropin-inhibitory hormone: what we know and what we still have to learn from fish. Front Endocrinol 10:78

    Google Scholar 

  10. Di Yorio MP, Sallemi JE, Toledo Solís FJ, Pérez Sirkin DI, Delgadin TH, Tsutsui K, Vissio PG (2018) Ontogeny of gonadotrophin-inhibitory hormone in the cichlid fish Cichlasoma dimerus. J Neuroendocrinol 30(6):e12608

    Google Scholar 

  11. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K (2006) Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.0511003103

    PubMed  Google Scholar 

  12. Kumar P, Wisdom KS, Bhat IA, Pathakota GB, Nayak SK, Reang D, Nagpure NS, Sharma R (2019) Molecular characterization of gonadotropin-inhibitory hormone (GnIH) gene and effect of intramuscular injection of GnIH peptide on the reproductive axis in Catla catla. Anim Biotechnol 8:1–5

    CAS  Google Scholar 

  13. Legagneux K, Bernard-Franchi G, Poncet F, La Roche A, Colard C, Fellmann D, Pralong F, Risold PY (2009) Distribution and genesis of the RFRP-producing neurons in the rat brain: comparison with melanin-concentrating hormone-and hypocretin-containing neurons. Neuropeptides 43(1):13–19

    CAS  PubMed  Google Scholar 

  14. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    CAS  PubMed  Google Scholar 

  15. Maddineni SR, Ocon-Grove OM, Krzysik-Walker SM, Hendricks GL, Ramachandran R (2008) Gonadotropin-inhibitory hormone (GnIH) receptor gene is expressed in the chicken ovary: potential role of GnIH in follicular maturation. Reproduction 135(2):267

    CAS  PubMed  Google Scholar 

  16. Muñoz-Cueto JA, Paullada-Salmerón JA, Aliaga-Guerrero M, Cowan ME, Ubuka PIST (2017) A journey through the gonadotropin-inhibitory hormone system of fish. Front Endocrinol. https://doi.org/10.3389/fendo.2017.00285

    Google Scholar 

  17. Ogawa S, Parhar I (2014) Structural and functional divergence of gonadotropin-inhibitory hormone (GnIH) from Jawless fish to mammals. Front Endocrinol 5:177

    Google Scholar 

  18. Osugi T, Daukss D, Gazda K, Ubuka T, Kosugi T, Nozaki M, Sower SA, Tsutsui K (2012) Evolutionary origin of the structure and function of gonadotropin-inhibitory hormone: insights from lampreys. Endocrinology 153(5):2362–2374

    CAS  PubMed  Google Scholar 

  19. Paullada-Salmerón JA, Cowan M, Aliaga-Guerrero M, Morano F, Zanuy S, Muñoz-Cueto JA (2016) Gonadotropin inhibitory hormone down-regulates the brain-pituitary reproductive axis of male European Sea Bass (Dicentrarchus labrax). Biol Reprod. https://doi.org/10.1095/biolreprod.116.139022

    PubMed  PubMed Central  Google Scholar 

  20. Paullada-Salmerón JA, Loentgen GH, Cowan M, Aliaga-Guerrero M, Rendón-Unceta MD, Muñoz-Cueto JA (2017) Developmental changes and day-night expression of the gonadotropin-inhibitory hormone system in the European sea bass: effects of rearing temperature. Comp Biochem Physiol A Mol Integr Physiol 206:54–62

    PubMed  Google Scholar 

  21. Peng W, Cao M, Chen J, Li Y, Wang Y, Zhu Z (2016) GnIH plays a negative role in regulating GtH expression in the common carp, Cyprinus carpio L. Gen Comp Endocrinol. https://doi.org/10.1016/j.ygcen.2016.06.001

    PubMed  Google Scholar 

  22. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol Lett 26(6):509–515

    CAS  PubMed  Google Scholar 

  23. Pinelli C, Jadhao AG, Bhoyar RC, Tsutsui K, D’Aniello B (2019) Distribution of gonadotropin-inhibitory hormone (GnIH)-like immunoreactivity in the brain and pituitary of the frog (Pelophylax esculentus) during development. Cell Tissue Res 17:1–3

    Google Scholar 

  24. Poling MC, Kauffman AS (2015) Regulation and function of RFRP-3 (GnIH) neurons during postnatal development. Front Endocrinol 6:150

    Google Scholar 

  25. Qi X, Zhou W, Li S, Lu D, Yi S, Xie R, Liu X, Zhang Y, Lin H (2013) Evidences for the regulation of GnRH and GTH expression by GnIH in the goldfish, Carassius auratus. Mol Cell Endocrinol 366(1):9–20

    CAS  PubMed  Google Scholar 

  26. Sandvik GK, Hodne K, Haug TM, Okubo K, Weltzien FA (2014) RFamide peptides in early vertebrate development. Front Endocrinol 5:203

    Google Scholar 

  27. Shahjahan M, Ikegami T, Osugi T, Ukena K, Doi H, Hattori A (2011) Synchronised expressions of LPXRFamide peptide and its receptor genes: seasonal, diurnal and circadian changes during spawning period in grass puffer. J Neuroendocrinol. https://doi.org/10.1111/j.1365-2826.2010.02081.x

    PubMed  Google Scholar 

  28. Tobari Y, Iijima N, Tsunekawa K, Osugi T, Okanoya K, Tsutsui K (2010) Identification of gonadotropin-inhibitory hormone in the zebra finch (Taeniopygia guttata): peptide isolation, cDNA cloning and brain distribution. Peptides. https://doi.org/10.1016/j.peptides.2010.01.015

    PubMed  Google Scholar 

  29. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275(2):661–667

    CAS  PubMed  Google Scholar 

  30. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ (2012) Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinol 153:373–385

    CAS  Google Scholar 

  31. Ubuka T, Kim S, Huang YC, Reid J, Jiang J, Osugi T (2008) Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology. https://doi.org/10.1210/en.2007-0983

    PubMed  PubMed Central  Google Scholar 

  32. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, Cadigan PA (2009) Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol 517:841–855

    CAS  PubMed  Google Scholar 

  33. Ubuka T, McGuire NL, Calisi RM, Perfito N, Bentley GE (2008) The control of reproductive physiology and behavior by gonadotropin-inhibitory hormone. Integr Comp Biol 48(5):560–569

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H (2009) Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS ONE 4:e8400

    PubMed  PubMed Central  Google Scholar 

  35. Ubuka T, Son YL, Bentley GE, Millar RP, Tsutsui K (2013) Gonadotropin-inhibitory hormone (GnIH), GnIH receptor and cell signaling. Gen Comp Endocrinol. https://doi.org/10.1016/j.ygcen.2013.02.030

    PubMed  Google Scholar 

  36. Ubuka T, Ueno M, Ukena K, Tsutsui K (2003) Developmental changes in gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica) hypothalamo-hypophysial system. J Endocrinol 178(2):311–318

    CAS  PubMed  Google Scholar 

  37. Ukena K, Iwakoshi-Ukena E, Osugi T, Tsutsui K (2016) Identification and localization of gonadotropin-inhibitory hormone (GnIH) orthologs in the hypothalamus of the red-eared slider turtle, Trachemysscripta elegans. Gen Comp Endocrinol 227:69–76

    CAS  PubMed  Google Scholar 

  38. Ukena K, Koda A, Yamamoto K, Kobayashi T, Iwakoshi-Ukena E, Minakata H (2003) Novel neuropeptides related to frog growth hormone-releasing peptide: isolation, sequence, and functional analysis. Endocrinol 144:3879–3884

    CAS  Google Scholar 

  39. Wang B, Yang G, Liu Q, Qin J, Xu Y, Li W (2017) Inhibitory action of tongue sole LPXRFa, the piscine ortholog of gonadotropin-inhibitory hormone, on the signaling pathway induced by tongue sole kisspeptin in COS-7 cells transfected with their cognate receptors. Peptides. https://doi.org/10.1016/j.peptides.2017.07.014

    PubMed  Google Scholar 

  40. Wang B, Zhang Y, Xu Y, Liu X, Cui A, Shi B, Jiang Y (2019) Developmental expression of LPXRFa, kisspeptin, and their receptor mRNAs in the half-smooth tongue sole Cynoglossus semilaevis. Fish Sci 85(3):449–455

    CAS  Google Scholar 

  41. Wang Q, Qi X, Guo Y, Li S, Zhang Y, Liu X (2015) Molecular identification of GnIH/GnIHR signal and its reproductive function in protogynous hermaphroditic orange-spotted grouper (Epinephelus coioides). Gen Comp Endocrinol. https://doi.org/10.1016/j.ygcen.2015.04.016

    PubMed  Google Scholar 

  42. Yano T, Iijima N, Hinuma S, Tanaka M, Ibata Y (2004) Developmental expression of RFamide-related peptides in the rat central nervous system. Dev Brain Res 152:109–120

    CAS  Google Scholar 

  43. Zhang Y, Li S, Liu Y, Lu D, Chen H, Huang X (2010) Structural diversity of the GnIH/GnIH receptor system in teleost: Its involvement in early development and the negative control of LH release. Peptides. https://doi.org/10.1016/j.peptides.2010.03.003

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Director & Vice-Chancellor, ICAR-Central Institute of Fisheries Education, Mumbai, India for providing support and necessary facilities for carrying out this experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rupam Sharma.

Ethics declarations

Conflict of interest

All authors declare that they no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 212 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, P., Wisdom, K.S., Kumar, G. et al. Ontogenetic and tissue-specific expression of gonadotropin-inhibitory hormone (GnIH) and its receptors in Catla catla. Mol Biol Rep 47, 3281–3290 (2020). https://doi.org/10.1007/s11033-020-05388-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-020-05388-5

Keywords

Navigation