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Pooja Kumari Neeta Sehgal S. V. Goswami Neerja Aggarwal

Abstract

Several external and internal factors contribute to the reproductive success of teleosts, which makes the reproductive process complex and unique. In the Indian freshwater catfish, Heteropneustes fossilis, monsoon plays a crucial role as it fine tunes the neuroendocrine axis, culminating in oocyte maturation. Therefore, induction of oocyte maturation requires the coordinated interaction among hypothalamic, hypophyseal, and peripheral hormones.  In the present investigation, dual neuroendocrine control of oocyte maturation has been demonstrated in the catfish, H. fossilis. The maturational response in gravid catfish is inhibited in the presence of dopamine but GnRH evokes the oocyte maturation and ovulation. GnRH upregulates the expression of lhb gene as well as increases plasma levels of LH significantly within 30 minutes of its administration. Destruction of the preoptic region in gravid catfish by electrolytic or chemical lesions also causes oocyte maturation and ovulation. But this response is inhibited if dopamine is injected into the nucleus preopticus periventricularis-lesioned fishes. These observations support the role of dopamine as an inhibitory factor, therefore specific receptors of dopamine have been characterized in catfish and their expression in the brain has been quantified. Dopamine receptors are upregulated in dopamine-treated fishes and downregulated if a dopamine antagonist (pimozide) is injected. The present study suggests the presence of inhibitory mechanism for LH secretion in gravid catfish. Abolition of this inhibition is necessary to release LH surge, which in turn stimulates resumption of meiosis and ovulation. Thus peptidergic as well as aminergic systems regulate oocyte maturation in H. fossilis. Neuroendocrine regulation of oocyte maturation and ovulation has major implications for inducing spawning in aquaculture.

Article Details

Article Details

Keywords

Dopamine, GnRH, Lesioning, Monosodium L-glutamate, Pimozide

References
Aggarwal, N., Goswami, S. & Sehgal, N. (2012). A stereotaxic atlas and technique for nuclei of the diencephalon of catfish, Heteropneustes fossilis (Bloch). J Env Bio-Sci, 26, 15.
Aizen, J., Meiri, I., Tzchori, I., Levavi-Sivan, B. & Rosenfeld, H. (2005). Enhancing spawning in the grey mullet (Mugil cephalus) by removal of dopaminergic inhibition. General and Comparative Endocrinology, 142, 212-221. https://doi.org/10.1016/j.ygcen.2005.01.002
Azuadi, N., Siraj, S., Daud, S., Christianus, A., Harmin, S., Sungan, S. & Britin, R.( 2011). Enhancing ovulation of Malaysian mahseer (Tor tambroides) in captivity by removal of dopaminergic inhibition. Journal of Fisheries and Aquatic Science, 6, 740.
Beriotto, A. C., Di Yorio, M. P., Sirkin, D. I. P., Toledo-Solis, F. J., Peña-Marín, E. S., Álvarez-González, C. A., & Vissio, P. G. (2020). Gonadotropin-inhibitory hormone (GnIH) distribution in the brain of the ancient fish Atractosteus tropicus (Holostei, Lepisosteiformes). General and Comparative Endocrinology, 299, 113623. https://doi.org/10.1016/j.ygcen.2020.113623
Bhat, S. K. & Ganesh, C. B. (2019). Dopamine receptor agonist bromocriptine restrains the follicular development, hatchling success and puberty in Gambusia affinis. Journal of Applied Ichthyology, 35(2), 501-511. https://doi.org/10.1111/jai.13875
Blázquez, M., Bosma, P., Fraser, E., Van Look, K. & Trudeau, V. (1998). Fish as models for the neuroendocrine regulation of reproduction and growth. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 119, 345-364. https://doi.org/10.1016/S0742-8413(98)00023-1
Bryant, A. S., Greenwood, A. K., Juntti, S. A., Byrne, A. E. & Fernald, R. D. (2016). Dopaminergic inhibition of gonadotropin-releasing hormone neurons in the cichlid fish Astatotilapia burtoni. J. Exp. Biol., 219, 3861-3865. https://doi.org/10.1242/jeb.147637
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem, 162, 156-9. https://doi.org/10.1016/0003-2697(87)90021-2
Ciani, E., Fontaine, R., Maugars, G., Nourizadeh-Lillabadi, R., Andersson, E., Bogerd, J., Von Krogh, K. & Weltzien, F.-A. (2020). Gnrh receptor gnrhr2bb? is expressed exclusively in lhb-expressing cells in Atlantic salmon male parr. General and Comparative Endocrinology, 285, 113293. https://doi.org/10.1016/j.ygcen.2019.113293
Corio, M., Peute, J. & Steinbusch, H. W. (1991). Distribution of serotonin- and dopamine-immunoreactivity in the brain of the teleost Clarias gariepinus. J Chem Neuroanat, 4, 79-95. https://doi.org/10.1016/0891-0618(91)90033-9
Drori, S., Ofir, M., Levavi-Sivan, B. & Yaron, Z. (1994). Spawning induction in common carp (Cyprinus carpio) using pituitary extract or GnRH superactive analogue combined with metoclopramide: analysis of hormone profile, progress of oocyte maturation and dependence on temperature. Aquaculture, 119, 393-407. https://doi.org/10.1016/0044-8486(94)90303-4  
Dufour, S., Sebert, M. E., Weltzien, F. A., Rousseau, K. & Pasqualini, C. (2010). Neuroendocrine control by dopamine of teleost reproduction. J Fish Biol, 76, 129-60. https://doi.org/10.1111/j.1095-8649.2009.02499.x
Dufour, S., Weltzien, F. A., Sebert, M. E., Le Belle, N., Vidal, B., Vernier, P. & Pasqualini, C. (2005). Dopaminergic inhibition of reproduction in teleost fishes: ecophysiological and evolutionary implications. Annals of the New York Academy of Sciences, 1040, 9-21. doi: 10.1196/annals.1327.002
El-Hawarry, W. N., Abd El-Rahman, S. H. & Shourbela, R. M. (2016). Breeding response and larval quality of African catfish (Clarias gariepinus, Burchell 1822) using different hormones/hormonal analogues with dopamine antagonist. The Egyptian Journal of Aquatic Research, 42, 231-239. https://doi.org/10.1016/j.ejar.2016.06.003
Fallah, H. P. & Habibi, H. R. (2020). Role of GnRH and GnIH in paracrine/autocrine control of final oocyte maturation. General and Comparative Endocrinology, 299, 113619. https://doi.org/10.1016/j.ygcen.2020.113619
Fallah, H. P., Rodrigues, M. S., Corchuelo, S., Nóbrega, R. H. & Habibi, H. R. (2020). Role of GnRH isoforms in paracrine/autocrine control of zebrafish (Danio rerio) spermatogenesis. Endocrinology, 161(2), bqaa004. https://doi.org/10.1210/endocr/bqaa004
Fontaine, R., Affaticati, P., Yamamoto, K., Jolly, C., Bureau, C., Baloche, S., Gonnet, F., Vernier, P., Dufour, S. & Pasqualini, C. (2013). Dopamine inhibits reproduction in female zebrafish (Danio rerio) via three pituitary D2 receptor subtypes. Endocrinology, 154, 807-18. https://doi.org/10.1210/en.2012-1759
Golan, M., Zelinger, E., Zohar, Y. & Levavi-Sivan, B. (2015). Architecture of GnRH-Gonadotrope-Vasculature Reveals a Dual Mode of Gonadotropin Regulation in Fish. Endocrinology, 156, 4163-73. https://doi.org/10.1210/en.2015-1150
Goswami, S. V. & Sundararaj, B. I. (1971). In vitro maturation and ovulation of oocytes of the catfish, Heteropneustes fossilis (Bloch): effects of mammalian hypophyseal hormones, catfish pituitary homogenate, steroid precursors and metabolites, and gonadal and adrenocortical steroids. J. Exp. Zool, 178, 467-77. https://doi.org/10.1002/jez.1401780405
Kah, O., Dulka, J. G., Dubourg, P., Thibault, J. & Peter, R. E. (1987). Neuroanatomical substrate for the inhibition of gonadotrophin secretion in goldfish: existence of a dopaminergic preoptico-hypophyseal pathway. Neuroendocrinology, 45, 451-8. https://doi.org/10.1159/000124774
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol., 35, 1547-1549. 10.1093/molbev/msy096
Kumari, P., Kumar, M., Sehgal, N. & Aggarwal, N. (2020). In silico analysis of kiss2, expression studies and protein–protein interaction with gonadotropin-releasing hormone 2 (GnRH2) and luteinizing hormone beta (LH?) in Heteropneustes fossilis. Journal of Biomolecular Structure and Dynamics, 1-15. https://doi.org/10.1080/0739 1102.20 20.1860820
Lamba, V. J., Goswami, S. V. & Sundararaj, B. I. (1983). Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17 beta, estrone, and testosterone) correlated with the annual gonadal cycle in the catfish, Heteropneustes fossilis (Bloch). Gen Comp Endocrinol, 50, 205-25. https://doi.org/10.1016/0016-6480(83)90221-6
Levavi-Sivan, B., Aizen, J. & Avitan, A. (2005). Cloning, characterization and expression of the D2 dopamine receptor from the tilapia pituitary. Mol Cell Endocrinol, 236, 17-30. https://doi.org/10.1016/j.mce.2005.03.010
Li, X., Zheng, S., & Wu, G. (2020). Nutrition and metabolism of glutamate and glutamine in fish. Amino acids, 52, 671-691. https://doi.org/10.1007/s00726-020-02851-2
Linard, B., Bennani, S. & Saligaut, C. (1995). Involvement of estradiol in a catecholamine inhibitory tone of gonadotropin release in the rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol, 99, 192-6. https://doi.org/10.1006/gcen.1995.1101
Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2? ??CT method. methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Maugars, G., Pasquier, J., Atkinson, C., Lafont, A. G., Campo, A., Kamech, N. & Rousseau, K. (2020). Gonadotropin-inhibitory hormone in teleosts: New insights from a basal representative, the eel. General and comparative endocrinology, 287, 113350. https://doi.org/10.1016/j.ygcen.2019.113350
Mylonas, C. C. & Zohar, Y. (2007). Promoting oocyte maturation, ovulation and spawning in farmed fish. The Fish Oocyte. Springer. https://doi.org/10.1007/978-1-4020-6235-3_15
Nagahama, Y. & Yamashita, M. (2008). Regulation of oocyte maturation in fish. Development, growth and differentiation, 50, S195-S219. https://doi.org/10.1111/j.1440-169X.2008.01019.x
Nocillado, J. N., Levavi-Sivan, B., Carrick, F. & Elizur, A. (2007). Temporal expression of G-protein-coupled receptor 54 (GPR54), gonadotropin-releasing hormones (GnRH), and dopamine receptor D2 (drd2) in pubertal female grey mullet, Mugil cephalus. Gen Comp Endocrinol, 150, 278-87. https://doi.org/10.1016/j.ygcen.2006.09.008
Paullada-Salmeron, J. A., Cowan, M., Aliaga-Guerrero, M., Morano, F., Zanuy, S. & Munoz-Cueto, J. A. (2016). Gonadotropin Inhibitory Hormone Down-Regulates the Brain-Pituitary Reproductive Axis of Male European Sea Bass (Dicentrarchus labrax). Biol Reprod, 94, 121. https://doi.org/10.1095/biolreprod.116.139022
Pavlick, R. J. & Moberg, G. P. (1997). Dopaminergic influence on gonadotropin secretion in white sturgeon (Acipenser transmontanus). Fish Physiology and Biochemistry, 16, 35-43.
Peter, R. & Yu, K. (1997). Neuroendocrine regulation of ovulation in fishes: basic and applied aspects. Reviews in Fish Biology and Fisheries, 7, 173-197. https://doi.org/10.1023/A:1018431610220
Peter, R. E., Crim, L. W., Goos, H. J. & Crim, J. W. (1978). Lesioning studies on the gravid female goldfish: neuroendocrine regulation of ovulation. Gen Comp Endocrinol, 35, 391-401. https://doi.org/10.1016/0016-6480(78)90133-8
Peter, R. E. & Paulencu, C. R. (1980). Involvement of the preoptic region in gonadotropin release-inhibition in goldfish, Carassius auratus. Neuroendocrinology, 31, 133-41. https://doi.org/10.1159/000123064
Podhorec, P. & Kouril, J. (2009). Induction of final oocyte maturation in Cyprinidae fish by hypothalamic factors: a review. Veterinarni Medicina, 54, 97-110.
Rainis, S. & Ballestrazzi, R. (2005). The control of reproduction in finfish species through GnRH treatments. Italian Journal of Animal Science, 4, 345-353. https://doi.org/10.4081/ijas.2005.345
Saligaut, C., Linard, B., Breton, B., Anglade, I., Bailhache, T., Kah, O. & Jego, P. (1999). Brain aminergic systems in salmonids and other teleosts in relation to steroid feedback and gonadotropin release. Aquaculture, 177, 13-20. https://doi.org/10.1016/S0044-8486(99)00065-4
Sloley, B. D., Kah, O., Trudeau, V. L., Dulka, J. G. & Peter, R. E. (1992). Amino acid neurotransmitters and dopamine in brain and pituitary of the goldfish: involvement in the regulation of gonadotropin secretion. J Neurochem, 58, 2254-62.  https://doi.org/10.1111/j.1471-4159.199 2.tb10971.x
Spicer, O. S., Zmora, N., Wong, T. T., Golan, M., Levavi-Sivan, B., Gothilf, Y. & Zohar, Y. (2017). The gonadotropin-inhibitory hormone (Lpxrfa) system's regulation of reproduction in the brain–pituitary axis of the zebrafish (Danio rerio). Biology of reproduction, 96(5), 1031-1042. https://doi.org/10.1093/biolre/iox032
Sundararaj, B. I. & Vasal, S. (1976). Photoperiod and temperature control in the regulation of reproduction in the female catfish Heteropneustes fossilis. Journal of the Fisheries Board of Canada, 33, 959-973.  https://doi.org/10.1139/f76-123
Sundararaj, B. I. & Viswanathan, N. (1971). Hypothalamo-hypophyseal neurosecretory and vascular systems in the catfish, Heteropneustes fossilis (Bloch). J Comp Neurol, 141, 95-106. https://doi.org/10.1002/cne.901410108
Vacher, C., Ferrière, F., Marmignon, M.-H., Pellegrini, E. & Saligaut, C. (2002). Dopamine D2 receptors and secretion of FSH and LH: role of sexual steroids on the pituitary of the female rainbow trout. General and comparative endocrinology, 127, 198-206. https://doi.org/10.1016/S0016-6480(02)00046-1
Yamamoto, K., Fontaine, R., Pasqualini, C. & Vernier, P. (2015). Classification of Dopamine Receptor Genes in Vertebrates: Nine Subtypes in Osteichthyes. Brain Behav Evol, 86, 164-75. https://doi.org/10.1159/000441550
Yamamoto, N., Parhar, I. S., Sawai, N., Oka, Y. & Ito, H. (1998). Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neuroscience research, 31, 31-38. https://doi.org/10.1016/S0168-0102(98)00022-4
Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Elizur, A. & Levavi-Sivan, B. (2003). Regulation of fish gonadotropins. Int Rev Cytol, 225, 131-85. https://doi.org/10.1016/S0074-7696(05)25004-0
Zohar, Y., Munoz-Cueto, J. A., Elizur, A. & Kah, O. (2010). Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol, 165, 438-55. https://doi.org/10.1016/j.ygcen.2009.04.017
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Research Articles

How to Cite

Multifactorial control of gonadotropin release for induction of oocyte maturation: Influence of gonadotropin-releasing hormone, gonadotropin release-inhibiting factor and dopamine receptors in the catfish, Heteropneustes fossilis. (2021). Journal of Applied and Natural Science, 13(2), 686-699. https://doi.org/10.31018/jans.v13i2.2695