Abstract
Several methods have been used to accelerate previtellogenesis and vitellogenesis stages in fish, including hormonal induction, sustained-release delivery systems, and oral delivery of gonadotropin-releasing hormone (GnRH). In this study, we proposed the oral administration of GnRH analog + nanoparticles of chitosan to accelerate oogenesis in goldfish as a model fish in reproductive biology and aquaculture. In this regard, adult female goldfish were fed with six experimental groups: chitosan, 50 μg GnRHa/kg b.w., 100 μg GnRHa/kg b.w., chitosan + 50 μg GnRHa/kg b.w., and chitosan + 100 μg GnRHa/kg b.w., and diet without any additive as the control for 40 days in triplicate. Every 10 days, ovarian samples were collected, and gonadosomatic index (GSI), oocyte diameter (OD), zona radiata thickness (Zr), and diameter of the follicular layer (Fl) were measured to assess ovarian developmental stage for each treatment. Additionally, blood sampling was done to measure serum 17β-estradiol concentration at the end of the experiment. All parameters remained unchanged during the experiment in the chitosan-fed group. In the group fed with 100 μg GnRH or chitosan nanoparticle + 100 μg GnRHa, these parameters in general were increased. However, the effects in 50 μg GnRHa or chitosan nanoparticle + 50 μg GnRHa treatments were uncertain; they affected serum E2 levels as a trend toward a significant increase was observed in goldfish treated with chitosan nanoparticle + 100 μg GnRHa. Finally, the results indicated the oral administration of chitosan + 100 μg GnRHa/kg b.w. significantly accelerated the oocyte development and growth of ovary.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aizenshtadt TB (1988) Oocyte Growth and Vitellogenesis In: "Oocyte growth and maturation". T. A. Dettlaff, S. G. Vassetzky, Frank Billett, (eds)
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. Gen Comp Endocrinol 142:212–221. https://doi.org/10.1016/J.YGCEN.2005.01.002
Alishahi A, Mirvaghefi A, Tehrani MR, Farahmand H, Koshio S, Dorkoosh FA, Elsabee MZ (2011) Chitosan nanoparticle to carry vitamin C through the gastrointestinal tract and induce the non-specific immunity system of rainbow trout (Oncorhynchus mykiss). Carbohydr Polym 86:142–146. https://doi.org/10.1016/J.CARBPOL.2011.04.028
Barannikova IA, Bayunova LV, Semenkova TB (2006) Serum sex steroids and their specific cytosol binding in the pituitary and gonads of Russian sturgeon (Acipenser gueldenstaetdii Brandt) during final maturation. J Appl Ichthyol 22:331–333. https://doi.org/10.1111/j.1439-0426.2007.00979.x
Bernkop-Schnürch A, Kast CE (2001) Chemically modified chitosans as enzyme inhibitors. Adv Drug Deliv Rev 52:127–137. https://doi.org/10.1016/s0169-409x(01)00196-x
Bernkop-Schnürch A, Weithaler A, Albrecht K, Greimel A (2006) Thiomers: Preparation and in vitro evaluation of a mucoadhesive nanoparticulate drug delivery system. Int J Pharm 317:76–81. https://doi.org/10.1016/J.IJPHARM.2006.02.044
Breton B, Roelants Y, Ollevier F, Epler P, Mikolajczyk T (1998) Improved bioavailability of orally delivered peptides and polypeptides in teleost fish. J Appl Ichthyol 14:251–257. https://doi.org/10.1111/j.1439-0426.1998.tb00651.x
Campbell B, Dickey J, Beckman B, Young G, Pierce A, Fukada H, Swanson P (2006) Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic-acute regulatory protein and receptors for gonadotropins, growth hormone, and somatolactin1. Biol Reprod 75:34–44. https://doi.org/10.1095/biolreprod.105.049494
Harmin SA, Crim LW, Wiegand MD (1995) Manipulation of the seasonal reproductive cycle in winter flounder, Pleuronectes americanus, using a gonadotropic hormone releasing hormone. Mar Biol 121:611–619. https://doi.org/10.1007/BF00349296
Ilium L (1998) Chitosan and its use as a pharmaceutical excipient. Pharm Res 15:1326–1331. https://doi.org/10.1023/A:1011929016601
Jackson K, Hurvitz A, Din SY, Goldberg D, Pearlson O, Degani G, Levavi-Sivan B (2006) Anatomical, hormonal and histological descriptions of captive Russian sturgeon (Acipenser gueldenstaedtii) with intersex gonads. Gen Comp Endocrinol 148:359–367. https://doi.org/10.1016/J.YGCEN.2006.04.008
Kean T, Thanou M (2010) Biodegradation, biodistribution and toxicity of chitosan. Adv Drug Deliv Rev 62:3–11. https://doi.org/10.1016/J.ADDR.2009.09.004
Levavi-Zermonsky B, Yaron Z (1986) Changes in gonadotropin and ovarian steroids associated with oocytes maturation during spawning induction in the carp. Gen Comp Endocrinol 62:89–98. https://doi.org/10.1016/0016-6480(86)90097-3
Linares-Casenave J, Kroll KJ, Van Eenennaam JP, Doroshov SI (2003) Effect of ovarian stage on plasma vitellogenin and calcium in cultured white sturgeon. Aquaculture 221:645–656. https://doi.org/10.1016/S0044-8486(03)00134-0
Mojazi Amiri B, Maebayashi M, Hara A, Adachi S, Yamauchi K (1996) Ovarian development and serum sex steroid and vitellogenin profiles in the female cultured sturgeon hybrid, the bester. J Fish Biol 48:1164–1178. https://doi.org/10.1111/j.1095-8649.1996.tb01812.x
Morehead DT, Pankhurst NW, Ritar AJ (1998) Effect of treatment with LHRH analogue on oocyte maturation, plasma sex steroid levels and egg production in female striped trumpeter Latris lineata (Latrididae). Aquaculture 169:315–331. https://doi.org/10.1016/S0044-8486(98)00374-3
Mylonas CC, Fostier A, Zanuy S (2010) Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 165:516–534. https://doi.org/10.1016/j.ygcen.2009.03.007
Paykan Heyrati F (2010) Study on induction of oocyts of reared Bluga Huso huso in captivity in previtogenic stage by LHRH implant. phD Thesis, University of Tehran, Iran
Ravi Kumar MNV (2000) A review of chitin and chitosan applications. React Funct Polym 46:1–27. https://doi.org/10.1016/S1381-5148(00)00038-9
Schep LJ, Tucker IG, Young G, Ledger R, Butt AG (1999) Controlled release opportunities for oral peptide delivery in aquaculture. J Control Release 59:1–14. https://doi.org/10.1016/S0168-3659(98)00175-8
Schreck CB, Contreras-Sanchez W, Fitzpatrick MS (2001) Effects of stress on fish reproduction, gamete quality, and progeny☆☆Oregon Agricultural Experiment Station Technical Report Number 11578. In: Lee C-S, Donaldson EM (eds) Reproductive Biotechnology in Finfish Aquaculture. Elsevier, Amsterdam, pp 3–24
Şenel S, Kremer MJ, Kaş S, Wertz PW, Hıncal AA, Squier CA (2000) Enhancing effect of chitosan on peptide drug delivery across buccal mucosa. Biomaterials 21:2067–2071. https://doi.org/10.1016/S0142-9612(00)00134-4
Sukumasavin, N., Leelapatra, W., Mclean,, E., McLean E., Donaldson E.M. (1992) Orally induced spawning of Thai carp (Puntius gonionotus, Bleeker) following co-administration of des Gly10 (D-Arg6) sGnRH ethylamide and domperidone. J Fish Biol 40:477-479. https://doi.org/10.1111/j.1095-8649.1992.tb02595.x
van der Lubben IM, Verhoef JC, van Aelst AC, Borchard G, Junginger HE (2001) Chitosan microparticles for oral vaccination:: preparation, characterization and preliminary in vivo uptake studies in murine Peyer’s patches. Biomaterials 22:687–694. https://doi.org/10.1016/S0142-9612(00)00231-3, Chitosan microparticles for oral vaccination: preparation, characterization and preliminary in vivo uptake studies in murine Peyer's patches
Vazirzadeh A, Mojazi Amiri B, Yelghi S, Hajimoradloo A, Nematollahi MA, Mylonas CC (2011) Comparison of the effects of different methods of mammalian and salmon GnRHa administration on spawning performance in wild-caught female carp (Cyprinus carpio carpio) from the Caspian Sea. Aquaculture 320:123–128. https://doi.org/10.1016/j.aquaculture.2011.08.001
Zheng W, Stacey NE (1997) A steroidal pheromone and spawning stimuli act via different neuroendocrine mechanisms to increase gonadotropin and milt volume in male goldfishCarassius auratus. Gen Comp Endocrinol 105:228–238. https://doi.org/10.1006/gcen.1996.6825
Zohar Y (1989) Endocrinology and fish farming: aspects in reproduction, growth, and smoltification. Fish Physiol Biochem 7:395–405. https://doi.org/10.1007/BF00004734
Zohar Y, Mylonas CC (2001) Endocrine manipulations of spawning in cultured fish: from hormones to genes. Reproductive Biotechnology in Finfish Aquaculture 99–136. https://doi.org/10.1016/B978-0-444-50913-0.50009-6
Acknowledgements
The Dept. of Fisheries, University of Tehran, and Pharmaceutics Department, Tehran University of Medical Sciences, have supported this research. The present work also was supported in part by the Iran National Science Foundation. The authors wish to extend their thanks to all people who helped them in various ways, making this research possible.
Author information
Authors and Affiliations
Contributions
Kookaram K.: MSc student; these data are coming from his thesis.
Mojazi Amiri B.: Professor in the Dept. of Fisheries and the main supervisor for the student. He provided all the scientific suggestions and grants.
Dorkoosh F.A.: He is the second supervisor and provided scientific suggestions.
Nematollahi M.A.: He was the advisor for the work and provided scientific comments.
Mortazavian E. was the advisor for the scientific group.
Abed Elmdoust A.A. was the advisor for the scientific group.
Corresponding author
Ethics declarations
Ethics approval
The authors followed all applicable international, national, and/or institutional guidelines for the care and use of animals. All procedures were carried out in accordance with the Animal Care and Use Committee guidelines at the Faculty of Sciences of the University of Tehran (357, 8 November 2000).
Conflict of interest
The authors declare that they have no conflict of interest.
Code availability
Not applicable
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kookaram, K., Mojazi Amiri, B., Dorkoosh, F.A. et al. Effect of oral administration of GnRHa+nanoparticles of chitosan in oogenesis acceleration of goldfish Carassius auratus. Fish Physiol Biochem 47, 477–486 (2021). https://doi.org/10.1007/s10695-021-00926-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-021-00926-9