Abstract
This study was conducted to identify the possible effect of recombinant vertebrate ancient long (VAL) opsin as a non-visual “photoreceptor” in the deep brain of goldfish, Carassius auratus. In addition, we investigated the effects of green-wavelength light on the predictable reproductive function of VAL-opsin as a green-sensitive pigment in the deep brain. To determine this, we quantified changes in gonadotropin hormone (GTH) [GTHα, follicle stimulating hormone (FSH) and luteinizing hormone (LH)] and estrogen receptor (ER; ERα and ERβ) mRNA expression levels associated with goldfish reproduction as well as changes in plasma FSH, LH, and 17β-estradiol (E2) activities after injection of recombinant VAL-opsin protein in two concentrations (0.1 or 0.5 μg/g body mass) for 4 weeks (injection once weekly) and examined the possible impact of green-wavelength light (500, 520, and 540 nm) on the function of VAL-opsin. As a result, all parameters associated with reproduction significantly increased with time and light-emitting diode (LED) exposure. Based on these results, we suggested that VAL-opsin in the deep brain is involved in goldfish maturation, and it is possible that green-wavelength light improves the ability of VAL-opsin to promote maturation by increasing VAL-opsin expression.
Similar content being viewed by others
Abbreviations
- E2:
-
17β-estradiol
- FSH:
-
Follicle-stimulating hormone
- GTH:
-
Gonadotropin hormone
- HPG:
-
Hypothalamus-pituitary-gonad
- LH:
-
Luteinizing hormone
- LED:
-
Light-emitting diode
- VAL-opsin:
-
Vertebrate ancient long opsin
References
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
Bowman CJ, Kroll KJ, Gross TG, Denslow ND (2002) Estradiol-induced gene expression in largemouth bass (Micropterus salmoides). Mol Cell Endocrinol 196:67–77
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
Choi CY, Shin HS, Choi YJ, Kim NN, Lee J, Kil G-S (2012) Effects of LED light spectra on starvation-induced oxidative stress in the cinnamon clownfish Amphprion melanopus. Comp Biochem Physiol A 163:357–363
Davis LK, Visitacion N, Riley L, Hiramatsu N, Sullivan C, Hirano T, Gordon GE (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
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
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
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 motor neurons in the vertebrate brain. PLoS Biol 11:e1001585
García-Fernández JM, Cernuda-Cernuda R, Davies WIL, 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
Jenkins A, Munoz M, Tarttelin EE, Bellingham J, Foster RG, Hankins MW (2003) VA opsin, melanopsin, and an inherent light response within retinal interneurons. Curr Biol 13:1269–1278
Jung SJ, Kim NN, Choi YJ, Choi JY, Choi Y-U, Heo YS, Choi CY (2016) Effects of melatonin and green-wavelength LED light on the physiological stress and immunity of goldfish, Carassius auratus, exposed to high water temperature. Fish Physiol Biochem 42:1335–1346
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
Kim NN, Choi YJ, Shin HS, Lim JR, Han JM, Cho JH, Lee J, Kil GS, Choi CY (2014) The effect of LED light spectra on antioxidant system by thermal stress in goldfish, Carassius auratus. Mol Cell Toxicol 10:47–58
Kobayashi M, Morita T, Ikeguchi K, Yoshizaki G, Suzuki T, Watabe S (2006) In vivo biological activity of recombinant goldfish gonadotropins produced by baculovirus in silkworm larvae. Aquaculture 256:433–442
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
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
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
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
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
Moutsaki P, Bellingham J, Soni BG, David-Gray ZK, Foster RG (2000) Sequence, genomic structure and tissue expression of carp (Cyprinus carpio L.) vertebrate ancient (VA) opsin. FEBS Lett 473:316–322
Owen MAG, Davies SJ, Sloman KA (2010) Light colour influences the behaviour and stress physiology of captive tench (Tinca tinca). Rev Fish Biol Fish 20:375–380
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
Shin HS, Lee J, Choi CY (2011) Effects of LED light spectra on oxidative stress and the protective role of melatonin in relation to the daily rhythm of the yellowtail clownfish, Amphiprion clarkii. Comp Biochem Physiol A 160:221–228
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
Soni BG, Foster RG (1997) A novel and ancient vertebrate opsin. FEBS Lett 406:279–283
Villamizar N, Garcia-Alcazar A, Sánchez-Vázquez FJ (2009) Effect of light spectrum and photoperiod on the growth, development and survival of European sea bass (Dicentrarchus labrax) larvae. Aquaculture 292:80–86
Villamizar N, Vera LM, Foulkes NS, Sanchez-Vazquez FJ (2014) Effect of lighting conditions on zebrafish growth and development. Zebrafish 11:173–181
Yoshikawa T, Oishi T (1998) Extraretinal photoreception and circadian systems in nonmammalian vertebrates. Comp Biochem Physiol B 119:65–72
Acknowledgements
This work was supported by the National Research Foundation of Korea grant funded by the Korean government (2014R1A2A2A01002747), and “Development and commercialization of high density low temperature plasma based seawater sterilization pulification system” funded by the Ministry of Oceans and Fisheries, Korea.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Choi, J.Y., Choi, C.Y. Effects of recombinant vertebrate ancient long opsin on reproduction in goldfish, Carassius auratus: profiling green-wavelength light. Fish Physiol Biochem 44, 1027–1036 (2018). https://doi.org/10.1007/s10695-018-0490-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-018-0490-4