Skip to main content
Log in

Influence of endomorphins along the pituitary-ovary axis in the Mozambique Tilapia Oreochromis mossambicus

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Endomorphins (EM-1 and EM-2) are the tetrapeptides involved in pain and neuroendocrine responses with a high affinity for μ-opioid receptors in vertebrates. However, their role in fish reproduction is not clear. The aim of this study was to investigate the influence of EM-1 and EM-2 on the pituitary-ovary axis in the Mozambique tilapia Oreochromis mossambicus. The experimental set-up consisted of four groups, namely, initial controls, controls, EM-1- and EM-2-treated groups (n = 10 in each group consisting of two replicates). Although the number of stage IV (vitellogenic) follicles was significantly lower (P < 0.05) in controls compared to initial controls, the stage V (preovulatory) follicles were present in controls in contrast to their absence in initial controls. Treatment of 40 μg EM-1/0.1 ml saline/fish/day for 22 days resulted in significant increase (P < 0.05) in the number of stage I follicles compared to controls. While similar treatment of EM-2 did not significantly alter the number of stage I follicles compared to controls, the number of stage II follicles was significantly lower (P < 0.05) in this group compared to those of controls and EM-1 treated fish. The number of stage III and IV follicles did not significantly differ among controls, EM-1- and EM-2-treated groups. However, a significant reduction (P < 0.05) in the mean number of stage V follicles was observed in EM-1- and EM-2-treated fish compared to controls. These changes were concomitant with significant reduction (P < 0.05) in the intensity and the percent area of immunoreactivity of luteinizing hormone (LH) secreting cells in the proximal pars distalis (PPD) of the pituitary gland and significantly higher (P < 0.05) percent occurrence of follicular atresia in EM-1- and EM-2-treated fish compared to those of controls. Taken together, these results suggest an inhibitory effect for endomorphins along the pituitary–ovary axis, for the first time in fish.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acosta-Martinez M, Etgen AM (2002) Activation of μ-opioid receptors inhibits lordosis behavior in estrogen and progesterone-primed female rats. Horm Behav 41:88–100

    Article  CAS  Google Scholar 

  • Agirregoitia E, Peralta L, Mendoza R, Exposito A, Ereno ED, Matorras R, Agirregoitia N (2012) Expression and localization of opioid receptors during the maturation of human oocytes. Reprod BioMed Online 24:550–557

    Article  CAS  Google Scholar 

  • Barr GA, Zadina JE (1999) The ontogeny of endomorphin-1- and endomorphin-2-like immunoreactivity in rat brain and spinal cord. Ann N Y Acad Sci 897:145–153

    Article  CAS  Google Scholar 

  • Bhat SK, Ganesh CB (2019) Domperidone treatment attenuates stress‐induced suppression of reproduction in viviparous mosquitofish Gambusia affinis. J Fish Biol. https://doi.org/10.1111/jfb.14183.

    Article  Google Scholar 

  • Bujdoso E, Jaszberenyi M, Tomboly C, Toth G, Telegdy G (2001) Behavioral and neuroendocrine action of endomorphin-2. Peptides 22:1459–1463

    Article  CAS  Google Scholar 

  • Chabbi A, Ganesh CB (2012) Stress-induced inhibition of recruitment of ovarian follicles for vitellogenic growth and interruption of spawning cycle in the fish Oreochromis mossambicus. Fish Physiol Biochem 38:1521–1532. https://doi.org/10.1007/s10695-012-9643-z

    Article  CAS  PubMed  Google Scholar 

  • Chabbi A, Ganesh CB (2013) β-Endorphin-induced inhibition of vitellogenic follicular growth in the fish Oreochromis mossambicus: Evidence for opioidergic mediation of ovarian stress response. J Exp Zool A Ecol Genet Physiol 319:156–165. https://doi.org/10.1002/jez.1781

    Article  CAS  PubMed  Google Scholar 

  • Ciarcia G, Facchinetti F, Vallarino M (1994) Testicular activity in the lizard Podarcis sicula. J Endocrinol 143:565–571

    Article  CAS  Google Scholar 

  • Coventry TL, Jessop DS, Finn DP, Crabb MD, Kinoshita H, Harbuz MS (2001) Endomorphins and activation of the hypothalamo-pituitary-adrenal axis. J Endocrinol 169:185–193

    Article  CAS  Google Scholar 

  • Czapla MA, Champion HC, Zadina JE, Kastin AJ, Hackler L, Ge LJ, Kadowitz PJ (1998) Endomorphin 1 and 2, endogenous mu-opioid agonists, decrease systemic arterial pressure in the rat. Life Sci 62:PL175–PL179

    Article  CAS  Google Scholar 

  • Desjardins GC, Brawer JR, Beaudet A (1990) Distribution of mu, delta, and kappa opioid receptors in the hypothalamus of the rat. Brain Res 536:114–123

    Article  CAS  Google Scholar 

  • Duan L, Wang J, Sun X, Yang X, Shan L, Liu Y, Wang H (2016) The role and significance of endomorphin-1 and μ-opioid receptor in rats with endometriosis. Gynecol Endocrinol 32:912–915

    Article  CAS  Google Scholar 

  • Facchinetti F, Genazzani AR, Vallarino M, Pestarino M, Polzonetti-Magni A, Carnevali O, Ciarcia G, Fasano SD, Antonio M, Pierantoni R (1993) Opioids and testicular activity in the frog Rana esculenta. J Endocrinol 137:49–57

    Article  CAS  Google Scholar 

  • Faletti AG, Mastronardi CA, Lomniczi A, Seilicovich A, Gimeno M, McCann SM, Rettori V (1999) β-Endorphin blocks luteinizing hormone-releasing hormone release by inhibiting the nitric oxidergic pathway controlling its release. Proc Natl Acad Sci U S A 96:1722–1726

    Article  CAS  Google Scholar 

  • Fichna J, Janecka A, Costentin J, Do Rego JC (2007) The endomorphin system and its evolving neurophysiological role. Pharmacol Rev 59:88–123

    Article  CAS  Google Scholar 

  • Finger TE (1981) Fish that taste with their feet: Spinal sensory pathway in the sea robin, Prionotus carolinus. Biol Bull 161:154–161

    Google Scholar 

  • Ganesh CB (2014) Follicular development status and profile of 17β estradiol and cortisol levels during the spawning cycle in Oreochromis mossambicus (Peters). Indian J Fish 61:45–51

  • Ganesh CB, Chabbi A (2013) Naltrexone attenuates stress-induced suppression of LH secretion in the pituitary gland in the Cichlid fish Oreochromis mossambicus: evidence for the opioidergic mediation of reproductive stress response. Fish Physiol Biochem 39:627–636. https://doi.org/10.1007/s10695-012-9725-y

    Article  CAS  PubMed  Google Scholar 

  • Ganesh CB, Yajurvedi HN (2003) β-Endorphin disrupts seasonal and FSH-induced ovarian recrudescence in the lizard Mabuya carinata. Gen Comp Endocrinol 133:305–313

    Article  CAS  Google Scholar 

  • Gelman PL, Herrera NEG, Ortega MEM, Villanueva EB, Santillan CT, Juarez AS, Palma BA (2010) Endomorphin peptides: pharmacological and functional implications of these peptides in the brain of mammals. Salud Ment (Part 2) 33:257–272

  • Harrison C, Rowbotham DJ, Grandy DK, Lambert DG (2000) Endomorphin-1 induced desensitization and down-regulation of the recombinant mu-opioid receptor. Br J Pharmacol 131:1220–1226. https://doi.org/10.1038/sj.bjp.0703683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen HT, Cutter C, Hardy S, Lehman MN, Goodman RL (2003) Seasonal plasticity within the gonadotropin-releasing hormone system of the ewe: changes in identified GnRH inputs and glial association. Endocrinology 144:3663–3676

    Article  CAS  Google Scholar 

  • Kou ZZ, Wan FP, Bai Y, Li CY, Hu JC, Zhang GT, Zhang T, Chen T, Wang YY, Li H, Li YQ (2016) Decreased endomorphin-2 and μ-opioid receptor in the spinal cord are associated with painful diabetic neuropathy. Front Mol Neurosci 9:80. https://doi.org/10.3389/fnmol.2016.00080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leadem CA, Kalra SP (1985) Effects of endogenous opioid peptides and opiates on luteinizing hormone and prolactin secretion in ovariectomized rats. Neuroendocrinology 41:342–352

    Article  CAS  Google Scholar 

  • Leadem CA, Yagenova SV (1987) Effects of specific activation of mu-, delta- and kappa-opioid receptors on the secretion of luteinizing hormone and prolactin in the ovariectomized rat. Neuroendocrinology 45:109–117

    Article  CAS  Google Scholar 

  • Li ZH, Shan LD, Jiang XH, Guo SY, Yu GD, Hisamitsu T, Yin QZ (2001) Analgesic effect of endomorphin-1. Acta Pharmacol Sin 22:976–980

    CAS  PubMed  Google Scholar 

  • Martin-Schild S, Gerall AA, Kastin AJ, Zadina JE (1999) Differential distribution of endomorphin 1- and endomorphin 2-like immunoreactivities in the CNS of the rodent. J Comp Neurol 405:450-471

  • Olson GA, Olson RD, Kastin AJ (1992) Endogenous opiates:1991. Peptides 13:1247–1287

    Article  CAS  Google Scholar 

  • Parra-Gámez L, García-Hidalgo AA, Salazar-Juárez A, Antón B, Paredes RG (2009) Endomorphin-1, effects on male sexual behavior. Physiol Behav 97:98–101

    Article  Google Scholar 

  • Pierce TL, Wessendorf MW (2000) Immunocytochemical mapping of endomorphin-2-immunoreactivity in rat brain. J Chem Neuroanat 18:181–207

    Article  CAS  Google Scholar 

  • Polzonetti-Magni A, Facchinetti F, Carnevali O, Mosconi G, Pestarino M, Vallarino M, Ciarcia G (1994) Presence and steroidogenic activity of β-endorphin in the ovary of the lizard Podarcis sicula sicula (Raf.). Biol Reprod 50:1059–1065

    Article  CAS  Google Scholar 

  • Rodriguez Diaz MA, Candal E, Santos-Duran GN, Adrio F, Rodriguez-Moldes I (2011) Comparative analysis of Met-enkephalin, galanin and GABA immunoreactivity in the developing trout preoptic–hypophyseal system. Gen Comp Endocrinol 173:148–158

    Article  CAS  Google Scholar 

  • Sinchak K, Micevych PE (2001) Progesterone blockade of estrogen activation of μ-opioid receptors regulates reproductive behaviour. J Neurosci 21:5723–5729

    Article  CAS  Google Scholar 

  • Smith CJ, Haley SR (1988) Steroid profiles of the female Tilapia, Oreochromis mossambicus, and correlation witt oocyte growth and mouthbrooding behavior. Gen Comp Endocrinol 69:88–98

    Article  CAS  Google Scholar 

  • Vallarino M, Bucharles C, Facchinetti F, Vaudry H (1994) Immunocytochemical evidence for the presence of met-enkephalin and leu-enkephalin in distinct neurons in the brain of the elasmobranch fish Scyliorhinus canicula. J Comp Neurol 347:585–597

    Article  CAS  Google Scholar 

  • Vallarino M, Thoumas JL, Masini MA, Trabucchi M, Chartrel N, Vaudry H (1998) Immunohistochemical localization of enkephalins in the brain of the African lungfish, Protopterus annectens, provides evidence for differential distribution of met-enkephalin and leu-enkephalin. J Comp Neurol 396:275–287

    Article  CAS  Google Scholar 

  • Vijayalaxmi, Ganesh CB (2017a) Influence of leucine-enkephalin on pituitary-ovary axis of the cichlid fish Oreochromis mossambicus. Fish Physiol Biochem 43:1253–1264

    Article  CAS  Google Scholar 

  • Vijayalaxmi, Ganesh CB (2017b) Distribution of endomorphin-like-immunoreactive neurones in the brain of the cichlid fish Oreochromis mossambicus. J Neuroendocrinol 29:1–17

    Article  Google Scholar 

  • Wang YQ, Zhu CB, Wu GC, Cao XD, Wang Y, Cui DF (1999) Effects of orphanin FQ on endomorphin-1 induced analgesia. Brain Res 835:241–246

    Article  CAS  Google Scholar 

  • Wayne NL, Kuwahara K (2007) Beta-endorphin alters electrical activity of gonadotropin releasing hormone neurons located in the terminal nerve of the teleost medaka (Oryzias latipes). Gen Comp Endocrinol 150:41–47

    Article  CAS  Google Scholar 

  • Whitten RD, Martin-Schild S, Zadina JE, Albers HE (2001) Endomorphin 1-like immunoreactivity in the limbic system of Syrian hamsters (Mesocricetus auratus). Brain Res Bull 56:563–567

    Article  CAS  Google Scholar 

  • Zadina JE, Hackler L, Ge LJ, Kastin AJ (1997) A potent and selective endogenous agonist for the μ-opiate receptor. Nature 386:499–502

    Article  CAS  Google Scholar 

  • Zerani M, Gobbetti A (1992) In vivo and in vitro studies on effects of β-endorphin and naloxone on sex steroids in the water frog Rana esculenta. Acta Physiol Scand 146:271–279

    Article  CAS  Google Scholar 

Download references

Funding

The present study was supported by a grant from Science and Engineering Research Board–Department of Science and Technology (No. SR/SO/AS-052/2013), New Delhi, India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C.B Ganesh.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vijayalaxmi, Ganesh, C. Influence of endomorphins along the pituitary-ovary axis in the Mozambique Tilapia Oreochromis mossambicus. Fish Physiol Biochem 46, 429–438 (2020). https://doi.org/10.1007/s10695-019-00731-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00731-5

Keywords

Navigation