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Effects of neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) treatment on ovarian development of the sapphire devil, Chrysiptera cyanea

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Abstract

In the neuroendocrine system controlling fish reproduction, dopamine (DA) acts as a gonadotropin inhibitory factor and plays a role in regulating gonadal development of certain species. The present study examined the effects of chemical destruction of dopaminergic neurons in the brain on DA production and ovarian development in the sapphire devil Chrysiptera cyanea, a reef-associated damselfish. The avidin–biotin–peroxidase complex method using an antibody against tyrosine hydroxylase (TH), a critical enzyme in the DA synthesis pathway, identified a population of dopaminergic neurons with somata in the anteroventral preoptic nucleus of the diencephalon and fibers terminating in the proximal pars distalis of the pituitary. Maintaining fish in seawater containing 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) at 0.02 and 0.2 µg/mL for 2 days resulted in decreases in DA, 3,4-dihydroxyphenylacetic acid (DOPAC; DA metabolite), and DA metabolic rate in the whole brain. The number of TH-positive neurons in the diencephalon decreased after 0.02 µg/mL MPTP treatment for 2 days. These results suggest that MPTP treatment destroys TH-positive neurons in the diencephalon, thereby decreasing the synthesis and release of DA from the brain. This treatment rescued ovarian development in fish with artificially retracted ovaries during the spawning season. The gonadosomatic index of MPTP-treated fish 5 and 7 days after treatment was significantly higher than that of control fish. Oocytes in the vitellogenic stages were observed in the ovaries of MPTP-treated fish, but not in control fish. These results suggest that DA in the brain drives ovarian development in the sapphire devil.

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References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Badruzzaman M (2014) Studies on monoaminergic system in relation to environmental perception in the brain of coral reef fish. Dissertation, University of the Ryukyus

  • Badruzzaman M, Bapary MAJ, Takemura A (2013) Possible roles of photoperiod and melatonin in reproductive activity via changes in dopaminergic activity in the brain of a tropical damselfish, Chrysiptera cyanea. Gen Comp Endocrinol 194:240–247

    Article  CAS  PubMed  Google Scholar 

  • Bapary MAJ, Fainuulelei P, Takemura A (2009) Environmental control of gonadal development in the tropical damselfish Chrysiptera cyanea. Mar Biol Res 5:462–469

    Article  Google Scholar 

  • Bapary MAJ, Amin MN, Takeuchi Y, Takemura A (2011) The stimulatory effects of long wavelengths of light on the ovarian development in the tropical damselfish, Chrysiptera cyanea. Aquaculture 314:188–192

    Article  Google Scholar 

  • Bapary MAJ, Amin MN, Takemura A (2012) Food availability as a possible determinant for initiation and termination of reproductive activity in the tropical damselfish Chrysiptera cyanea. Mar Biol Res 8:154–162

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burns RS, Chiueh CC, Markey SP, Ebert MH, Jacobowitz DM, Kopin IR (1983) A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc Natl Acad Sci USA 80:4546–4550

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chang JP, Peter RE (1983) Effects of dopamine on gonadotropin release in female goldfish, Carassius auratus. Neuroendocrinology 36:351–357

    Article  CAS  PubMed  Google Scholar 

  • Chang JP, Yu KL, Wong AOL, Peter RE (1990) Differential actions of dopamine receptor subtypes on gonadotropin and growth hormone release in vitro in goldfish. Neuroendocrinology 51:664–674

    Article  CAS  PubMed  Google Scholar 

  • De Leeuw R, Goos HJTh, Van Oordt PGWJ (1986) The dopaminergic inhibition of the gonadotropin-releasing hormone-induced gonadotropin release: as in vitro study with fragments and cell suspensions from pituitaries of the African catfish, Clarias gariepinus (Burchell). Gen Comp Endocrinol 63:171–177

    Article  PubMed  Google Scholar 

  • De Leeuw R, Van’t Veer C, Goos HJ, Van Oordt PG (1988) The dopaminergic regulation of gonadotropin-releasing hormone receptor binding in the pituitary of the African catfish Clarias gariepinus. Gen Comp Endocrinol 72:408–415

    Article  PubMed  Google Scholar 

  • Dufour S, Lopez E, Le Menn F, Le Belle N, Baloche S, Fontaine YA (1988) Stimulation of gonadotropin release and of ovarian development, by the administration of a gonadoliberin agonist and of a dopamine antagonists, in female silver eel pretreated with estradiol. Gen Comp Endocrinol 70:20–30

    Article  CAS  PubMed  Google Scholar 

  • Dufour S, Weltzien FA, Sebert ME, Le Belle N, Vidal B, Vernier P, Pasqualini C (2005) Dopaminergic inhibition of reproduction in teleost fishes: ecophysiological and evolutionary implications. Ann NY Acad Sci 1040:9–21

    Article  CAS  PubMed  Google Scholar 

  • Dufour S, Sebert ME, Weltzien FA, Rousseau K, Pasqualini C (2010) Neuroendocrine control by dopamine of teleost reproduction. J Fish Biol 76:129–160

    Article  CAS  PubMed  Google Scholar 

  • 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 154:807–818

    Article  CAS  PubMed  Google Scholar 

  • Goping G, Pollard HB, Adeyemo OM, Kuijpers GAJ (1995) Effect of MPTP on dopaminergic neurons in the goldfish brain: a light and electron microscope study. Brain Res 687:35–52

    Article  CAS  PubMed  Google Scholar 

  • Groves DJ, Batten TFC (1986) Direct control of the gonadotroph in a teleost, Poecilia latipinna. II. Neurohormones and neurotransmitters. Gen Comp Endocrinol 62:315–326

    Article  CAS  PubMed  Google Scholar 

  • Heikkila RE, Hess A, Duvoisin RC (1984) Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice. Science 224:1451–1453

    Article  CAS  PubMed  Google Scholar 

  • Hibbert B, Fung I, McAuley R, Larivière K, MacNeil B, Bafi-Yeboa N, Livesey J, Trudeau V (2004) Increased GAD67 mRNA levels are correlated with in vivo GABA synthesis in the MPTP-treated catecholamine-depleted goldfish brain. Mol Brain Res 128:121–130

    Article  CAS  PubMed  Google Scholar 

  • Hibbert B, Fung I, McAuley R, Samia M, Trudeau V (2005) Catecholamine depletion modulates serum LH levels, GAD67 mRNA, and GABA synthesis in the goldfish. Gen Comp Endocrinol 140:176–183

    Article  CAS  PubMed  Google Scholar 

  • Hoque MM, Takemura A, Matsuyama M, Matsuura S, Takano K (1999) Lunar spawning in Siganus canaliculatus. J Fish Biol 55:1213–1222

    Article  Google Scholar 

  • Kah O, Dulka JG, Dubourg P, Thibault J, Peter RE (1987) Neuroanatomical substrate for the inhibition of gonadotropin secretion in goldfish: existence of a dopamine preoptic-hypophyseal pathway. Neuroendocrinology 45:451–458

    Article  CAS  PubMed  Google Scholar 

  • Kumakura N, Okuzawa K, Gen K, Kagawa H (2003) Effects of gonadotropin-releasing hormone agonist and dopamine antagonist on hypothalamus–pituitary–gonadal axis of pre-pubertal female red seabream (Pagrus major). Gen Comp Endocrinol 131:264–273

    Article  CAS  PubMed  Google Scholar 

  • Levavi-Sivan B, Safarian H, Rosenfeld H, Elizur A, Avitan A (2004) Regulation of gonadotropin-releasing hormone (GnRH)-receptor gene expression in tilapia: effect of GnRH and dopamine. Biol Reprod 70:1545–1551

    Article  CAS  PubMed  Google Scholar 

  • Levavi-Sivan B, Biran J, Fireman E (2006) Sex steroids are involved in the regulation of gonadotropin-releasing hormone and dopamine D2 receptors in female tilapia pituitary. Biol Reprod 75:642–650

    Article  CAS  PubMed  Google Scholar 

  • Lucchi R, Notari S, Pierantozzi S, Barnabei O, Villani L, Poli A (1998) Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in goldfish cerebellum: neurochemical and immunocytochemical analysis. Brain Res 782:105–112

    Article  CAS  PubMed  Google Scholar 

  • Masuda H, Amaoka K, Araga C, Uyeno T, Youshino T (1984) The fishes of the Japanese Archipelago. Tokai University Press, Tokyo

    Google Scholar 

  • Matsui H, Taniguchi Y, Inoue H, Uemura K, Takeda S, Takahashi R (2009) A chemical neurotoxin, MPTP induces Parkinson’s disease like phenotype, movement disorders and persistent loss of dopamine neurons in medaka fish. Neurosci Res 65:263–271

    Article  CAS  PubMed  Google Scholar 

  • McKinley ET, Baranowski TC, Blavo DO, Cato C, Doan TN, Rubinstein AL (2005) Neuroprotection of MPTP-induced toxicity in zebrafish dopaminergic neurons. Mol Brain Res 141:128–137

    Article  CAS  PubMed  Google Scholar 

  • Mok EYM, Munro AD (1998) Effects of dopaminergic drugs on locomotor activity in teleost fish of the genus Oreochromis (Cichlidae): involvement of the telencephalon. Physiol Behav 64:227–234

    Article  CAS  PubMed  Google Scholar 

  • Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229

    CAS  PubMed  Google Scholar 

  • Peng C, Gallin W, Peter RE, Blomqvist AG, Larhammar D (1994) Neuropeptide-Y gene expression in the goldfish brain: distribution and regulation by ovarian steroids. Endocrinology 134:1095–1103

    CAS  PubMed  Google Scholar 

  • Peter RE, Chang JP, Nahorniak CS, Omeljaniuk RJ, Sokolowska M, Shih SH, Billard R (1986) Interactions of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish. Recent Prog Horm Res 42:513–548

    CAS  PubMed  Google Scholar 

  • Petzinger GM, Fisher B, Hogg E, Abernathy A, Arevalo P, Nixon K, Jakowec MW (2006) Behavioral motor recovery in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned squirrel monkey (Saimiri sciureus): changes in striatal dopamine and expression of tyrosine hydroxylase and dopamine transporter proteins. J Neurosci Res 83:332–347

    Article  CAS  PubMed  Google Scholar 

  • Pham HQ, Arukwe A (2013) Effects of dopamine 2 receptor antagonist on sex steroid levels, oocyte maturation and spawning performances in Waigieu seaperch (Psammoperca waigiensis). Fish Physiol Biochem 39:403–411

    Article  CAS  PubMed  Google Scholar 

  • Podhorec P, Socha M, Sokolowska-Mikolajczyk M, Policar T, Svinger VW, Drozd B, Kouril J (2012) Dopamine control of LH release in the tench (Tinca tinca). Gen Comp Endocrinol 175:34–38

    Article  CAS  PubMed  Google Scholar 

  • Poli A, Guarnieri T, Facchinetti F, Villani L (1990) Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in goldfish brain. Brain Res 534:45–50

    Article  CAS  PubMed  Google Scholar 

  • Pollard HB, Dhariwal K, Adeyemo OM, Markey CJ, Levine CM, Markey S, Youdim MBH (1992) A parkinsonian syndrome induced in the goldfish by the neurotoxin MPTP. FASEB J 6:3108–3116

    CAS  PubMed  Google Scholar 

  • Rahman MS, Takemura A, Takano K (2000) Correlation between plasma steroid hormones and vitellogenin profiles and lunar periodicity in the female golden rabbitfish, Siganus guttatus (Bloch). Comp Biochem Physiol B 127:113–122

    Article  CAS  PubMed  Google Scholar 

  • Saligaut C, Linard B, Mañanos EL, Kah O, Breton B, Govoroun M (1998) Release of pituitary gonadotropins GtH I and GtH II in the rainbow trout (Oncorhynchus mykiss): modulation by estradiol and catecholamines. Gen Comp Endocrinol 109:302–309

    Article  CAS  PubMed  Google Scholar 

  • Takemura A, Uchimura M, Shibata Y (2010) Dopaminergic activity in the brain of a tropical wrasse in response to changes in light and hydrostatic pressure. Gen Comp Endocrinol 166:513–519

    Article  CAS  PubMed  Google Scholar 

  • Vidal B, Pasqualini C, Le Belle N, Holland MCH, Sbaihi M, Vernier P, Zohar Y, Dufour S (2004) Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: a neuroendocrine lock for the onset of puberty. Biol Reprod 71:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Weltzien FA, Pasqualini C, Sébert ME, Vidal B, Le Belle N, Kah O, Vernier P, Dufour S (2006) Androgen-dependent stimulation of brain dopaminergic systems in the female European eel (Anguilla anguilla). Endocrinology 147:2964–2973

    Article  CAS  PubMed  Google Scholar 

  • Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavi-Sivan B (2003) Regulation of fish gonadotropins. Int Rev Cytol 225:131–185

    Article  CAS  PubMed  Google Scholar 

  • Yu KL, Rosenblum PM, Peter RE (1991) In vitro release of gonadotropin-releasing hormone from the brain preoptic-anterior hypothalamic region and pituitary of female goldfish. Gen Comp Endocrinol 81:256–267

    Article  CAS  PubMed  Google Scholar 

  • Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165:438–455

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the staff of Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, for their technical assistance. This study was supported in part by a Grant-in-Aid for Scientific Research (A) (JSPS KAKENHI Grant Number: 23248033) and for Challenging Exploratory Research (JSPS KAKENHI Grant Number: 25660170) from the Japan Society for the Promotion of Science (JSPS) to AT.

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  1. Department of Chemistry, Biology and Marine Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    Muhammad Badruzzaman, Satoshi Imamura, Yuki Takeuchi, Taro Ikegami & Akihiro Takemura

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  1. Muhammad Badruzzaman
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  2. Satoshi Imamura
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  3. Yuki Takeuchi
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Correspondence to Akihiro Takemura.

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Badruzzaman, M., Imamura, S., Takeuchi, Y. et al. Effects of neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) treatment on ovarian development of the sapphire devil, Chrysiptera cyanea . Fish Physiol Biochem 41, 61–71 (2015). https://doi.org/10.1007/s10695-014-0006-9

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