Cloning and expression of melatonin receptors in the mudskipper Boleophthalmus pectinirostris: their role in synchronizing its semilunar spawning rhythm

Hong, Lu Yan; Hong, Wan Shu; Zhu, Wen Bo; Shi, Qiong; You, Xin Xin; Chen, Shi Xi

doi:10.1016/j.ygcen.2013.11.004

Cited by 34Circadian rhythm and melatoninReproductive biology and impacts on aquatic speciesHypothalamic control of reproductive hormones

Cloning and expression of melatonin receptors in the mudskipper Boleophthalmus pectinirostris: their role in synchronizing its semilunar spawning rhythm

Hong, Lu Yan, Hong, Wan Shu, Zhu, Wen Bo, Shi, Qiong, You, Xin Xin, Chen, Shi Xi·2014·General and Comparative Endocrinology

DOI 10.1016/j.ygcen.2013.11.004

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Abstract

The mudskipper Boleophthalmus pectinirostris, a burrow-dwelling fish inhabiting intertidal mudflats, spawns only once during the spawning season around either the first or last lunar quarters. To understand the molecular mechanisms regulating this semilunar spawning rhythm, we cloned all melatonin receptor subtypes (mtnr1a1.4, mtnr1a1.7, mtnr1b, and mtnr1c). Expression of three melatonin receptor subtypes (except mtnr1c) was found in the ovaries. In contrast, the expression of all receptor subtypes was found in the diencephalon and the pituitary. In the fully-grown follicles, only mtnr1a1.7 mRNA was detected in both the isolated follicle layers and denuded oocytes. Interestingly, the transcript levels of both mtnr1a1.4 in the diencephalon and mtnr1a1.7 in the ovary displayed two cycles within one lunar month, and peaked around the first and last lunar quarters. We used 17α,20β-dihydroxy-4-pregnen-3-one (DHP), a maturation-inducing hormone, as a biomarker to examine the involvement of melatonin receptors in the control of the spawning cycle. Melatonin significantly increased the plasma DHP level 1h post intraperitoneal injection. Melatonin also directly stimulated ovarian fragments in vitro to produce a significantly higher amount of DHP. Taken together, these results provided the first evidence that melatonin receptors were involved in the synchronization of the semilunar spawning rhythm in the female mudskipper by acting through the HPG axis and/or directly on ovarian tissues to stimulate the production of DHP.

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At least two melatonin receptors in the mudskipper Boleophthalmus pectinirostris fluctuate with semilunar periodicity, in phase with the aanat2 gene in the pineal.
“Moreover, at least two of the melatonin receptors in the mudskipper, Boleophthalmus pectinirostris fluctuate with semilunar periodicity, in phase with the aanat2 gene in the pineal of that species (40).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [40]

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Kim, N. N., Choi, Y., Park, H., & Choi, C. Y. (2014) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2014.08.020 · Cited by 10 · see citing works
Functional Involvement of Melatonin and Its Receptors in Reproductive Regulation of the Marine Teleost, Large Yellow Croaker (Larimichthys crocea)
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“These findings provide a foundation for investigating the connection between rhythmic patterns and reproductive processes in teleost fish, offering meaningful insights into melatonin’s diverse roles in fish reproduction for future research.”
The pineal and reproduction of teleosts and other fishes
Falcón, J., & Muñoz‐Cueto, J. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-16009-7.00008-6 · Cited by 7 · see citing works
A Crosstalk Between Pineal and Major Extra-Pineal Sources of Melatonin and its Role in Ovarian Growth and Maturation in Fish
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Cytoarchitecture of Mudskipper (Boleophthalmus pectinirostris) Brain
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“Previous studies indicated that melatonin may directly regulate the pituitary hormonal secretions: (1) Messenger RNA corresponding to melatonin receptors and/or melatonin binding sites have been identified in the pituitary of several fish species (Gaildrat and Falcón, 1999, 2000; Gaildrat et al., 2002; Park et al., 20…”
Background
Two pathways regulate insulin-like growth factor genes in the brain and liver of the tropical damselfish Chrysiptera cyanea: A possible role for melatonin in the actions of growth and thyroid hormones
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Expressions of melanopsins in telencephalon imply their function in synchronizing semilunar spawning rhythm in the mudskipper Boleophthalmus pectinirostris
Ma, H., Yang, M. S., Zhang, Y., Qiu, H. T., You, X., Chen, S. X., & Hong, W. (2021) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2021.113926 · Cited by 5 · see citing works
A progestin regulates the prostaglandin pathway in the neuroendocrine system in female mudskipper Boleophthalmus pectinirostris
Ma, H., Hong, W. ‐., & Chen, S. X. (2023) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2023.106300 · Cited by 3 · see citing works
Induction of spawning under artificial moonlight in the honeycomb grouper Epinephelus merra, a lunar-synchronized spawner
Fukunaga, K., Takeuchi, Y., Yamauchi, C., & Takemura, A. (2022) · Biological Rhythm Research · doi:10.1080/09291016.2022.2046416 · Cited by 3 · see citing works
“In addition, specific subtypes of melatonin receptors are expressed in the pituitary of mudskipper Boleophthalmus pectinirostris (Hong et al. 2014), orange-spotted grouper E. coioides (Chai et al. 2013), Atlantic salmon Salmo salar (Ciani et al. 2019), and medaka Oryzias latipes (Maugars et al.…”
Background
Potent Influence of Exogenous Melatonin on In Vitro Oocyte Maturation in the Longchin Goby, Chaenogobius annularis
Kim, D.-G., Hwang, I. J., & Baek, H. J. (2023) · Development & Reproduction · doi:10.12717/dr.2023.27.3.127 · Cited by 2 · see citing works
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Lunar Age-Dependent Oscillations in Expression of the Genes for Kisspeptin, GnIH, and Their Receptors in the Grass Puffer during the Spawning Season
Shahjahan, M., Rahman, M. L., Ohno, Y., Zahangir, M. M., & Ando, H. (2023) · ZOOLOGICAL SCIENCE · doi:10.2108/zs230061 · Cited by 2 · see citing works
“The lunar-age-dependent expression of melatonin receptor genes has been reported in the golden rabbitfish (Park et al., 2014) and mudskipper (Hong et al., 2014).”
Background
Melatonin influences reproduction in the sapphire devil Chrysiptera cyanea via regulation of dopamine 2b receptor transcription
Byun, J., Mahardini, A., Rizky, D., Udagawa, S., Fukunaga, K., Tan, E. S., Kim, J., Hur, S., & Takemura, A. (2024) · Frontiers in Marine Science · doi:10.3389/fmars.2024.1412148 · Cited by 1 · see citing works
Assembly of Two Small Body-Sized West Pacific Sciaenid GenomesPreprint
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Distinct roles of melatonin receptors in spermatogenesis in vitro in four-eyed sleeper (Bostrychus sinensis)
Yao, J., Li, H., Yang, H., Yi, M., & Liu, W. (2025) · Aquaculture Reports · doi:10.1016/j.aqrep.2025.103204
Investigating the roles behind four main corticosteroids in the reproductive cycle of female Eurasian perch Perca fluviatilis L. reared in RAS
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Photoperiodic regulation of reproduction and hypothalamic-pituitary-gonadal axis in Phoxinus lagowskii adults
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“…confirmed the expression of melatonin receptors in the ovaries of various bony fish species, including Catla catla (Chattoraj et al. 2009; Moniruzzaman and Maitra 2012), Boleophthalmus pectinirostris (Hong et al. 2014), Epinephelus coioides (Chai et al. 2013), and O. niloticus (Jin et al. 2013).”

Expressions of melanopsins in telencephalon imply their function in synchronizing semilunar spawning rhythm in the mudskipper Boleophthalmus pectinirostris
Ma, H., Yang, M. S., Zhang, Y., Qiu, H. T., You, X., Chen, S. X., & Hong, W. (2021) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2021.113926 · Cited by 5 · see citing works
Localization of Melatonin Receptor Mel_(1a) in Mudskipper(Boleophthalmus pectinirostris)
Qiyong, Z. (2012) · Journal of Xiamen University
Involvement of melatonin in transducing moon-related signals into the reproductive network of the female honeycomb grouper Epinephelus merra
Fukunaga, K., Yamashina, F., Ohta, N., Mizuno, H., Takeuchi, Y., Yamauchi, C., & Takemura, A. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113211 · Cited by 17 · see citing works
Distinct roles of melatonin receptors in spermatogenesis in vitro in four-eyed sleeper (Bostrychus sinensis)
Yao, J., Li, H., Yang, H., Yi, M., & Liu, W. (2025) · Aquaculture Reports · doi:10.1016/j.aqrep.2025.103204
Influence of moonlight on mRNA expression patterns of melatonin receptor subtypes in the pineal organ of a tropical fish
Park, Y.-J., Park, J., Takeuchi, Y., Hur, S., Lee, Y.-D., Kim, S.-J., & Takemura, A. (2013) · Marine Genomics · doi:10.1016/j.margen.2013.10.006 · Cited by 28 · see citing works

Authors: Hong, L. Y., Hong, W. S., Zhu, W. B., Shi, Q., You, X. X., & Chen, S. X.
Affiliations: Xiamen University (CN)
BGI Group (China) (CN)
Corresponding author: Chen, Shi Xi
ORCID: Shi, Qiong
You, Xin Xin
Chen, Shi Xi
Venue: General and Comparative Endocrinology
Publisher: Elsevier BV
Published: 2014-01
Volume: 195
Pages: 138-150
ISSN: 0016-6480 (ISSN-L)
DOI: 10.1016/j.ygcen.2013.11.004
OpenAlex: W2031912633
Cited by: 34
References: 62
Citations by year: 2026: 1 · 2025: 3 · 2024: 3 · 2023: 5 · 2022: 4 · 2021: 6 · 2020: 3 · 2019: 3 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 1
FWCI: 0.72
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: General and Comparative Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: National Natural Science Foundation of China (40976095, 31201977)
Key Project of Science and Technology of Fujian Province (2008N0041)
Xiamen University President Research Award (2013121044)
Shenzhen R & D Foundation for Science and Technology (CXB201108250095A)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords: melatonin receptors, Boleophthalmus pectinirostris, mudskipper, MTNR1B, ovarian follicle maturation, DHP, hypothalamic-pituitary-gonadal axis, diencephalon, pituitary gland
MeSH terms: Amino Acid Sequence, Animals, Cloning, Molecular, Female, Molecular Sequence Data, Ovary, Perciformes, Periodicity, Phylogeny, Reproduction, RNA, Messenger, Seasons, Tissue Distribution, Moon, Sequence Homology, Amino Acid, Reverse Transcriptase Polymerase Chain Reaction, Receptors, Melatonin, Real-Time Polymerase Chain Reaction

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Cloning and expression of melatonin receptors in the mudskipper Boleophthalmus pectinirostris: their role in synchronizing its semilunar spawning rhythm

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