Abstract
Vertebrate ancient long (VAL)-opsin is a green-sensitive photoreceptor that shows high sequence similarity to vertebrate ancient opsin, which is considered to play a role in sexual maturation via gonadotropin-releasing hormone (GnRH); however, the role of VAL-opsin in vertebrate sexual maturity remains unclear. Therefore, we investigated the possible role of VAL-opsin in reproduction in the goldfish Carassius auratus under a state of GnRH inhibition. Goldfish were injected with recombinant VAL-opsin protein (0.5 μg/g body mass) and/or the GnRH antagonist cetrorelix (0.5 μg/fish), and changes in the mRNA expression levels of genes associated with goldfish reproduction were measured by quantitative polymerase chain reaction, including those involved in the hypothalamus-pituitary-gonad (HPG) axis, VAL-opsin, GnRH, the gonadotropins (GTHs) luteinizing hormone and follicle-stimulating hormone, and estrogen receptor (ER). Moreover, the fish were irradiated with a green light-emitting diode (520 nm) to observe the synergistic effect on the HPG axis with VAL-opsin. Green LED exposure significantly and slightly increased the VAL-opsin and GnRH levels, respectively; however, these effects were blocked in groups injected with cetrorelix at all time points. Cetrorelix significantly decreased the mRNA levels of GTHs and ER, whereas these hormones recovered by co-treatment with VAL-opsin. These results indicate that green LED is an effective light source to promote the expression of sex hormones in fish. Moreover, VAL-opsin not only affects activity of the HPG axis but also appears to act on the pituitary gland directly to stimulate a new sexual maturation pathway that promotes the secretion of GTHs independent of GnRH.
Similar content being viewed by others
References
Behrens UD, Douglas RH, Sugden D, Davies DJ, Wagner HJ (2000) Effect of melatonin agonists and antagonists on horizontal cell spinule formation and dopamine release in a fish retina. Cell Tissue Res 299:299–306. https://doi.org/10.1007/s004419900161
Berardelli R, Gianotti L, Karamouzis I, Picu A, Giordano R, Angelo V, Zinnà D, Lanfranco F, Ghigo E, Arvat E (2011) Effects of cetrorelix, a GnRH-receptor antagonist, on gonadal axis in women with functional hypothalamic amenorrhea. Gynecol Endocrinol 27:753–758. https://doi.org/10.3109/09513590.2010.526661
Blanco-Vives B, Aliaga-Guerrero M, Canavate JP, Munoz-Cueto JA, Sanchez-Vazquez FJ (2011) Does lighting manipulation during incubation affect hatching rhythms and early development of sole? Chronobiol Int 28:300–306. https://doi.org/10.3109/07420528.2011.560316
Blaser RE, Rosemberg DB (2012) Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test. PLoS One 7:e36931. https://doi.org/10.1371/journal.pone.0036931
Bowman CJ, Kroll KJ, Gross TG, Denslow ND (2002) Estradiol-induced gene expression in largemouth bass (Micropterus salmoides). Mol Cell Endocrinol 196:67–77. https://doi.org/10.1016/S0303-7207(02)00224-1
Bustin SA, Benes V, Garson JA (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. https://doi.org/10.1373/clinchem.2008.112797
Choi JY, Choi CY (2018) Effects of recombinant vertebrate ancient long opsin on reproduction in goldfish, Carassius auratus: profiling green-wavelength light. Fish Physiol Biochem 44:1027–1036. https://doi.org/10.1007/s10695-018-0490-4
Choi CY, Shin HS, Kim NN, Yang SG, Kim BS, Yu YM (2015) Time-related effects of various LED light spectra on reproductive hormones in the brain of the goldfish Carassius auratus. Biol Rhythm Res 46:671–682. https://doi.org/10.1080/09291016.2015.1046247
Crim LW, Glebe BD (1990) Reproduction. In: Schreck CB, Moyle PB (eds) Methods for fish biology. Amer Fish Soc Bethesda, p 529–547
Davies WI, Turton M, Peirson SN, Follett BK, Halford S, Garcia-Fernandez JM, Sharp PJ, Hankins MW, Foster RG (2012) Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol Lett 8:291–294. https://doi.org/10.1098/rsbl.2011.0864
Davis LK, Visitacion N, Riley L, Hiramatsu N, Sullivan C, Hirano T, Gordon Grau E (2009) Effects of o,p’-DDE, heptachlor, and 17β-estradiol on vitellogenin gene expression and the growth hormone/insulin-like growth factor-I axis in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol C 149:507–514. https://doi.org/10.1016/j.cbpc.2008.11.007
Diedrich K, Diedrich C, Santos E, Zoll C, Al-Hasani S, Reissmann T, Klingmüller D (1994) Suppression of the endogenous luteinizing hormone surge by the gonadotrophin-releasing hormone antagonist cetrorelix during ovarian stimulation. Hum Reprod 9:788–791. https://doi.org/10.1093/oxfordjournals.humrep.a138597
Drivenes O, Soviknes AM, Ebbesson LO, Fjose A, Seo HC, Helvik JV (2003) Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. J Comp Neurol 456:84–93. https://doi.org/10.1002/cne.10523
Duncan NJ, Selkirk C, Porter M, Hunter D, Magwood S, Bromage N (2000) The effect of altered photoperiods on maturation of male and female Atlantic salmon (Salmo salar), observations of different responses and mechanisms. In: Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO (eds) Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. Bergen, Norway, p 344
Fischer RM, Fontinha BM, Kirchmaier S, Steger J, Bloch S, Inoue D, Panda S, Rumpel S, Tessmar-Raible K (2013) Co-expression of VAL- and TMT-opsins uncovers ancient photosensory interneurons and motorneurons in the vertebrate brain. PLoS Biol 11:e1001585. https://doi.org/10.1371/journal.pbio.1001585
Foster RG, Soni BG (1998) Extraretinal photoreceptors and their regulation of temporal physiology. Rev Reprod 3:145–150. https://doi.org/10.1530/revreprod/3.3.145
Gábor M, Marilena M (2009) Luteinizing hormone-releasing hormone antagonists. Expert Opin Ther Pat 19:1771–1785. https://doi.org/10.1016/S0090-4295(01)01238-9
Ganesh CB (2017) Influence of leucine-enkephalin on pituitary-ovary axis of the cichlid fish Oreochromis mossambicus. Fish Physiol Biochem 43:1253–1264. https://doi.org/10.1007/s10695-017-0369-9
García-Fernández JM, Cernuda-Cernuda R, Davies WI, Rodgers J, Turton M, Peirson SN, Follett BK, Halford S, Hughes S, Hankins MW, Foster RG (2015) The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin. Front Neuroendocrinol 37:13–28. https://doi.org/10.1016/j.yfrne.2014.11.001
Grandi G, Colombo G, Chicca M (2003) Immunocytochemical studies on the pituitary gland of Anguilla anguilla L., in relation to early growth stages and diet-induced sex differentiation. Gen Comp Endocrinol 131:66–76. https://doi.org/10.1016/S0016-6480(02)00646-9
Halford S, Pires SS, Turton M, Zheng L, González-Menéndez I, Davies WL, Perison SN, García-Fernández JM, Hankins MW, Foster RG (2009) VA opsin-based photoreceptors in the hypothalamus of birds. Curr Biol 19:396–1402. https://doi.org/10.1016/j.cub.2009.06.066
Karakatsouli N, Papoutsoglou ES, Sotiropoulosa N, Mourtikasa D, Stigen-Martinsena T, Papoutsoglou SE (2010) Effects of light spectrum, rearing density and light intensity on growth performance of scaled and mirror common carp Cyprinus carpio reared under recirculating system conditions. Aqauculture 42:121–127. https://doi.org/10.1016/j.aquaeng.2010.01.001
Kim MH, Oka Y, Amano M, Kobayashi M, Okuzawa K, Hasegawa Y, Kawashima S, Suzuki Y, Aida K (1995) Immunocytochemical localization of sGnRH and cGnRH-II in the brain of goldfish, Carassius auratus. J Comp Neurol 356:72–82. https://doi.org/10.1016/j.cbpb.2012.04.006
Kobayashi T, Nishizawa K,Mitsumori, K (2006) Individual variation of hormonal recovery after cessation of luteinizing hormone-releasing hormone agonist therapy in men receiving long-term medical castration therapy for prostate cancer. Scand J Urol Nephrol 40:98–203. https://doi.org/10.1080/00365590600641533
Kojima D, Mano H, Fukada Y (2000) Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci 20:2845–2851. https://doi.org/10.1523/JNEUROSCI.20-08-02845.2000
Kojima D, Torii M, Fukada Y, Dowling JE (2008) Differential expression of duplicated VAL-opsin genes in the developing zebrafish. J Neurochem 104:1364–1371. https://doi.org/10.1111/j.1471-4159.2007.05093.x
Lee YH, Du JL, Yen FP, Lee CY, Dufour S, Huang JD, Sun LT, Chang CF (2001) Regulation of plasma gonadotropin II secretion by sex steroids, aromatase inhibitors, and antiestrogens in the protandrous black porgy, Acanthopagrus schlegeli Bleeker. Comp Biochem Physiol B 129:399–406. https://doi.org/10.1016/S1096-4959(01)00337-2
Migaud H, Taylor JF, Taranger GL, Davie A, Cerda-Reverter JM, Carrillo M, Hansen T, Bromage NB (2006) A comparative ex vivo and in vivo study of day and night perception in teleosts species using the melatonin rhythm. J Pineal Res 41:42–52. https://doi.org/10.1111/j.1600-079X.2006.00330.x
Minamoto T, Shimizu I (2002) A novel isoform of vertebrate ancient opsin in a smelt fish, Plecoglossus altivelis. Biochem Biophys Res Commun 290:280–286. https://doi.org/10.1006/bbrc.2001.6186
Nagahama Y, Yoshikuni M, Yamashita M, Tokumoto T, Katsu Y (1995) Regulation of oocyte growth and maturation in fish. Curr Top Dev Biol 30:103–45. https://doi.org/10.1016/s0070-2153(08)60565-7
Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, Ebihara S, Kubo Y (2010) A mammalian neural tissues opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci 107:15264–15268. https://doi.org/10.1073/pnas.1006393107
Owen MAG, Davies SJ, Sloman KA (2010) Light colour influences the behaviour and stress physiology of captive tench (Tinca tinca). Rev Fish Biol Fisher 20:375–380. https://doi.org/10.1007/s11160-009-9150-1
Pankhurst NW, Thomas PM (1998) Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout Oncorhynchus mykiss to luteinizing hormone releasing hormone analogue. Aquaculture 166:163–177. https://doi.org/10.1080/00365590600641533
Pechstein B, Nagaraja NV, Hermann R, Romeis P, Locher M, Derendorf H (2000) Pharmacokinetic-pharmacodynamic modeling of testosterone and luteinizing hormone suppression by cetrorelix in healthy volunteers. J Clin Pharmacol 40:266–274. https://doi.org/10.1177/00912700022008937
Pierce LX, Noche RR, Ponomareva O, Chang C, Liang JO (2008) Novel function for period 3 and Exo-rhodopsin in rhythmic transcription and melatonin biosynthesis within the zebrafish pineal organ. Brain Res 1223:11–24. https://doi.org/10.1016/j.brainres.2008.05.020
Reissmann T, Schally AV, Bouchard P, Riethmuller H, Engel J (2000) The LHRH antagonist cetrorelix: a review. Hum Reprod Update 6:322–331. https://doi.org/10.1093/humupd/6.4.322
Song JA, Kim NN, Choi YJ, Choi JY, Kim B-S, Choi CY (2016) Effects of light-emitting diode spectra on the vertebrate ancient long opsin and gonadotropin hormone in the goldfish Carassius auratus. Biochem Biophys Res Commun 476:541–545. https://doi.org/10.1016/j.bbrc.2016.05.159
Soni BG, Foster RG (1997) A novel and ancient vertebrate opsin. FEBS Lett 406:279–283. https://doi.org/10.1016/S0014-5793(97)00287-1
Villamizar N, Vera LM, Foulkes NS, Sanchez-Vazquez FJ (2014) Effect of lighting conditions on zebrafish growth and development. Zebrafish 11:173–181. https://doi.org/10.1089/zeb.2013.0926
Funding
This work was supported by the National Research Foundation of Korea grant funded by the Korean government (MSIP) (2018R1A2B6002569).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests.
Human and animal rights
All handling and experimental protocols with fish complied with ethical guidelines in accordance with the Animal Protection Act and were approved by the Institutional Animal Care Use Committee of Korea.
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
Choi, J.Y., Choi, C.Y. Gonadotropin-releasing hormone-independent effects of recombinant vertebrate ancient long opsin in the goldfish Carassius auratus reveal alternative reproduction pathways. Fish Physiol Biochem 46, 1219–1227 (2020). https://doi.org/10.1007/s10695-020-00784-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-020-00784-x