Temporal expression of thyroid hormone regulating genes (tsh-b, tsh-r, dio2 and dio3) and their correlation with annual reproductive cycle of the Indian freshwater catfish, Heteropneustes fossilis (Bloch).
##plugins.themes.bootstrap3.article.main##
Abstract
Photoperiod and temperature are well-established environmental cues for gonadal growth in seasonally reproducing organisms. The photoperiod is known to regulate seasonal reproduction via induction of thyroid hormone regulating genes in the saccus vasculosus (SV) of fishes. However, SV is absent in many seasonally breeding fishes, including Heteropneustes fossilis. H. fossilis is a long-day breeding catfish in which gonadal recrudescence begins six months earlier than spawning. The present study attempted to analyse the expression of thyroid hormone-regulating genes (tsh-b, tsh-r, dio2 and dio3) in the brain, liver and ovary. In the brain, upregulated expression of thyrotropin-beta subunit (tsh-b), deiodinase2 (dio2) and deiodinase3 (dio3) genes is concomitant with the increasing photoperiod and temperature in nature, which may appear to regulate seasonal reproduction. Both deiodinases, dio2 and dio3, were also upregulated in the liver and ovarian tissue during the gonadal growth phase. The upregulation of deiodinases may enhance the metabolism and activity of tissues, thereby facilitating their respective roles. The expression of these genes was also assessed in the brain, liver, ovary, kidney, skin, spleen and gill tissues during the spawning period. The ubiquitous expression of deiodinases may point to enhanced activity in their organ-specific role. The present study speculates that expression of tsh-b, tsh-r, dio2 and dio3 genes during the reproductive phase of H. fossilis might be involved in the regulation of seasonal reproduction.
##plugins.themes.bootstrap3.article.details##
##plugins.themes.bootstrap3.article.details##
Keywords
Deiodinase enzymes, Saccus vasculosus, Seasonal reproduction, Thyroid, Thyrotropin
References
Bianco, A. C., Salvatore, D., Gereben, B., Berry, M. J. & Larsen, P. R. (2002). Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocrine Reviews, 23(1), 38-89. https://doi.org/10.1210/edrv.23.1.0455.
Chang, J., Hao, W., Xu, Y., Xu, P., Li, W., Li, J. & Wang, H. (2018). Stereoselective degradation and thyroid endocrine disruption of lambda-cyhalothrin in lizards (Eremias argus) following oral exposure. Environmental Pollution, 232, 300-309. https://doi.org/10.1016/j.envpol.2017.09.072
Chaube, R. & Joy, K. P. (2002). Effects of altered photoperiod and temperature, serotonin-affecting drugs, and melatonin on brain tyrosine hydroxylase activity in female catfish, Heteropneustes fossilis: A study correlating ovarian activity changes. Journal of Experimental Zoology, 293(6), 585–593.https://doi.org/10.1002/jez.10185
Chaube, R., Sharma, S., Senthilkumaran, B., Bhat, S. G. & Joy, K. P. (2020). Expression profile of kisspeptin2 and gonadotropin-releasing hormone2 mRNA during photo-thermal and melatonin treatments in the female air-breathing catfish Heteropneustes fossilis. Fish Physiology and Biochemistry, 46(6), 2403-2419. https://doi.org/10.10 07/s10695-020-00888-4
Chaube, R., Sharma, S., Senthilkumaran, B., Bhat, S. G. & Joy, K. P. (2022). Kisspeptins stimulate the hypothalamus-pituitary-ovarian axis and induce final oocyte maturation and ovulation in female stinging catfish (Heteropneustes fossilis): Evidence from in vivo and in vitro studies. Aquaculture, 548, 737734. https://doi.org/10.1 016/j.aquaculture.2021.737734
Chi, L., Li, X., Liu, Q. & Liu, Y. (2017). Photoperiod regulate gonad development via kisspeptin/kissr in hypothalamus and saccus vasculosus of Atlantic salmon (Salmo salar). PloS one, 12(2), e0169569. https://doi.org/10.1371/journal.pone.01 69569
Chi, L., Li, X., Liu, Q. & Liu, Y. (2019). Photoperiod may regulate growth via leptin receptor A1 in the hypothalamus and saccus vasculosus of Atlantic salmon (Salmo salar). Animal Cells and Systems, 23(3), 200-208. . https://doi.org/10.10 80/19768354.2019.1595138
Chomczynski, P. & Sacchi, N. (2006). The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on. Nature Protocols, 1(2), 581–585.https://doi.org/10.1038/nprot.2006.83
Cyr, D. G. & Eales, J. G. (1988). Influence of thyroidal status on ovarian function in rainbow trout, Salmo gairdneri. Journal of Experimental Zoology, 248(1), 81–87. https://doi.org/10.1002/jez.140248 0110
Cyr, D. G., Idler, D. R., Audet, C., McLeese, J. M. & Eales, J. G. (1998). Effects of long-term temperature acclimation on thyroid hormone deiodinase function, plasma thyroid hormone levels, growth, and reproductive status of male atlantic cod, Gadus morhua. General and Comparative Endocrinology, 109(1), 24–36.https://doi.org/10.1006/gcen.19 97.6994
Deal, C. K. & Volkoff, H. (2021). Response of the thyroid axis and appetite-regulating peptides to fasting and overfeeding in goldfish (Carassius auratus). Molecular and Cellular Endocrinology, 528, 111229. https://doi.org/10.1016/j.mce.20 21.11122 9
Doyle, A., Cowan, M. E., Migaud, H., Wright, P. J. & Davie, A. (2021). Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 260, 111000. https://doi.org/10.1016/j.cbpa.2021.111000
Eales, J. G. & Brown, S. B. (1993). Measurement and regulation of thyroidal status in teleost fish. Reviews in Fish Biology and Fisheries, 3(4), 299–347. https://doi.org/10.1007/BF00043383
Eales, J. G. (2019). The relationship between ingested thyroid hormones, thyroid homeostasis and iodine metabolism in humans and teleost fish. General and Comparative Endocrinology, 280, 62-72. https://doi.org/10.1016/j.ygcen.2019.04.012
Falcon, J., Migaud, H., Muñoz-Cueto, J. A. & Carrillo, M. (2010). Current knowledge on the melatonin system in teleost fish. General and Comparative Endocrinology, 165(3), 469–482. https://doi.org/10.1016/j.ygcen.2009.04.026
Feng, N. Y., Marchaterre, M. A. & Bass, A. H. (2019). Melatonin receptor expression in vocal, auditory, and neuroendocrine centers of a highly vocal fish, the plainfin midshipman (Porichthys notatus). Journal of Comparative Neurology, 527(8), 1362-1377. https://doi.org/10.1002/cne.24629
Fleming, M. S., Maugars, G., Lafont, A. G., Rancon, J., Fontaine, R., Nourizadeh-Lillabadi, R., Weltzien, F. A., Yebra-Pimentel, E. S., Dirks, R., McCormick, S. D., Rousseau, K., Martin, P. & Dufour, S. (2019). Functional divergence of thyrotropin beta-subunit paralogs gives new insights into salmon smoltification metamorphosis. Scientific Reports, 9(1), 1–15. https://doi.org/10.1038/s41598-019-40019-5
Fournie, J. W., Wolfe, M. J., Wolf, J. C., Courtney, L. A., Johnson, R. D. & Hawkins, W. E. (2005). Diagnostic criteria for proliferative thyroid lesions in bony fishes. Toxicologic Pathology, 33(5), 540–551. https://doi.org/10.1080/01926230500214509
Galton, V. A. (1992). Thyroid hormone receptors and iodothyronine deiodinases in the developing Mexican axolotl, Ambystoma mexicanum. General and Comparative Endocrinology, 85(1), 62–70. https://doi.org/10.1016/0016-6480(92)90172-G
Garcia, I., Garcia de Souza, J., Plaul, S. E., Miranda, L. & Colautti, D. (2022). Effect of photoperiod and temperature on ovarian maturation in the small characid fish Cheirodon interruptus. Journal of Applied Aquaculture, 1-13. https://doi.org/10.10 80/10454438.2022.2047867
Germain, D. L. S. & Galton, V. A. (1997). The deiodinase family of selenoproteins. Thyroid, 7(4), 655-668. https://doi.org/10.1089/thy.1997.7.655
Goto-Kazeto, R., Kazeto, Y. & Trant, J. M. (2003). Cloning and seasonal changes in ovarian expression of a TSH receptor in the channel catfish, Ictalurus punctatus. Fish Physiology and Biochemistry, 28(1), 339-340. https://doi.org/10.1023/B:FISH.0000030578.25321.8f
Guh, Y. J., Tamai, T. K. & Yoshimura, T. (2019). The underlying mechanisms of vertebrate seasonal reproduction. Proceedings of the Japan Academy, Series B, 95(7), 343-357. https://doi.org/10.2183/pjab.95.025
Hafeez, M. & Ahmad, I. (2021). Melatonin and Seasonal Reproduction in Teleosts. In Recent updates in molecular Endocrinology and Reproductive Physiology of Fish (pp. 181-192). Springer, Singapore. https://doi.org/10.1007/978-981-15-8369-8_13
Hsu, S. Y., Liang, S. G. & Hsueh, A. J. (1998). Characterization of two LGR genes homologous to gonadotropin and thyrotropin receptors with extracellular leucine-rich repeats and a G protein-coupled, seven-transmembrane region. Molecular endocrinology, 12(12), 1830-1845. https://doi.org/10.1210/mend.12.12.0211
Hughes, T. E. & McNABB, F. M. A. (1986). Avian hepatic T-3 production by two pathways of 5′-monodeiodination: Effects of fasting and patterns during development. 238:393-399. https://doi.org/10.1002/jez.1402380312
Hur, S. P., Mahardini, A., Takeuchi, Y., Imamura, S., Wambiji, N., Rizky, D. & Takemura, A. (2020). Expression profiles of types 2 and 3 iodothyronine deiodinase genes in relation to vitellogenesis in a tropical damselfish, Chrysiptera cyanea. General and Comparative Endocrinology, 285, 113264. https://doi.org/10.1016/j.ygcen.2019.113264
Husse, J., Eichele, G. & Oster, H. (2015). Synchronization of the mammalian circadian timing system: Light can control peripheral clocks independently of the SCN clock: Alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time. Bioessays, 37(10), 1119–1128. https://doi.org/10.1002/bies.20 1500026
Ikegami, K., Liao, X. H., Hoshino, Y., Ono, H., Ota, W., Ito, Y., Nishiwaki-Ohkawa, T., Sato, C., Kitajima, K., Iigo, M., Shigeyoshi, Y., Yamada, M., Murata, Y., Refetoff, S. & Yoshimura, T. (2014). Tissue-specific posttranslational modification allows functional targeting of thyrotropin. Cell Reports, 9(3), 801–809. https://doi.org/10.1016/j.celrep.201 4.10.0 06
Irachi, S., Hall, D. J., Fleming, M. S., Maugars, G., Dufour, S., Uchida, K. & Mccormick, S. D. (2021). Photoperiodic regulation of pituitary thyroid-stimulating hormone and brain deiodinase in Atlantic salmon. Molecular and Cellular Endocrinology, 519. https://doi.org/10.1016/j.mce.2020.111056
Köhrle, J. & Frädrich, C. (2022). Deiodinases control local cellular and systemic thyroid hormone availability. Free Radical Biology and Medicine. https://doi.org/10.1016/j.freeradbiomed.202 2.09.024
Kohrle, J. (1999). Local activation and inactivation of thyroid hormones: The deiodinase family. Molecular and Cellular Endocrinology, 151(1–2), 103–119. https://doi.org/10.1016/S0303-7207(99)00040-4
Köhrle, J. (2000). The deiodinase family: Selenoenzymes regulating thyroid hormone availability and action. Cellular and Molecular Life Sciences, 57(13–14), 1853–1863. https://doi.org/10.1007/PL00000667
Kupprat, F., Hölker, F. & Kloas, W. (2020). Can skyglow reduce nocturnal melatonin concentrations in Eurasian perch? Environmental Pollution, 262, 114324. https://doi.org/10.1016/j.envpol.2020.11 4324
Kwonm, J. Y., Chang, Y. J., Sohn, Y. C. & Aida, K. (1999). Plasma and ovarian thyroxine levels in relation to sexual maturation and gestation in female Sebastes inermis. Journal of Fish Biology, 54(2), 370–379. . https://doi.org/10.1111/j.1095-8649.1999.tb00836.x
Lalli, E. & Sassone-Corsi, P. (1995). Thyroid-stimulating hormone (TSH)-directed induction of the CREM gene in the thyroid gland participates in the long-term desensitization of the TSH receptor. Proceedings of the National Academy of Sciences of the United States of America, 92(21), 9633–9637. https://doi.org/10.1073/pnas.92.21.9633
Laslo, M., Denver, R. J. and Hanken, J. (2019). Evolutionary conservation of thyroid hormone receptor and deiodinase expression dynamics in ovo in a direct-developing frog, Eleutherodactylus coqui. Frontiers in endocrinology, 10, 307. https://doi.org/10.3389/fendo.2019.00307
Leiner, K. A., Han, G. S. & MacKenzie, D. S. (2000). The effects of photoperiod and feeding on the diurnal rhythm of circulating thyroid hormones in the red drum, Sciaenops ocellatus. General and Comparative Endocrinology, 120(1), 88–98. https://doi.org/10.1006/gcen.2000.7539
Lepine, M. & Verreault, J. (2022). Biotransformation of Dec-604 and potential effect on thyroid deiodinase activity in highly flame retardant-exposed gulls. Environmental Research, 215, 114268. https://doi.org/10.1016/j.envres.2022.1 14268
Li, Z. H., Li, P. & Wu, Y. (2021). Effects of temperature fluctuation on endocrine disturbance of grass carp Ctenopharyngodon idella under mercury chloride stress. Chemosphere, 263,128137.https://doi.org/10.1016/j.chemosphere.2020.128137
Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.20 01.1262
Lorgen, M., Casadei, E., Król, E., Douglas, A., Birnie, M. J., Ebbesson, L. O. E., Nilsen, T. O., Jordan, W. C., Jørgensen, E. H., Dardente, H., Hazlerigg, D. G. & Martin A.m, S. (2015). Functional divergence of type 2 deiodinase paralogs in the Atlantic salmon. Current Biology, 25(7), 936–941. https://doi.org/10.1016/j.cub.2015.01.074
Luongo, C., Dentice, M. & Salvatore, D. (2019). Deiodinases and their intricate role in thyroid hormone homeostasis. Nature Reviews Endocrinology, 15(8), 479-488.
Ma, Y., Ladisa, C., Chang, J. P. & Habibi, H. R. (2020). Seasonal related multifactorial control of pituitary gonadotropin and growth hormone in female goldfish: Influences of neuropeptides and thyroid hormone. Frontiers in endocrinology, 11, 175. https://doi.org/10.3389/fendo.2020.00175
MacLatchy, D. L. & Eales, J. G. (1992). Properties of T4 5′-deiodinating systems in various tissues of the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology, 86(2), 313–322. https://doi.org/10.1016/0016-6480(92)90116-2
MacLatchy, D. L., Kawauchi, H. & Eales, J. G. (1992). Stimulation of hepatic thyroxine 5’-deiodinase activity in rainbow trout (Oncorhynchus mykiss) by Pacific salmon growth hormone.., 101(4), 689–691. https://doi.org/10.1016/0300-9629(92)90344-p
Maeda, R., Shimo, T., Nakane, Y., Nakao, N. & Yoshimura, T. (2015). Ontogeny of the saccus vasculosus, a seasonal sensor in fish. Endocrinology, 156(11), 4238-4243. https://doi.org/10.1210/en.2015-1415
Mahardini, A., Rizky, D., Byun, J. H., Yamauchi, C., Takeuchi, Y. & Takemura, A. (2020). Food availability alters expression profiles of genes in relation to reproduction and nutrition in the females of tropical damselfish (Chrysiptera cyanea). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 333(9), 619-628. https://doi.org/10.1002/jez.2409
Marcinkowski, P., Hoyer, I., Specker, E., Furkert, J., Rutz, C., Neuenschwander, M. & Krause, G. (2019). A new highly thyrotropin receptor-selective small-molecule antagonist with potential for the treatment of Graves' orbitopathy. Thyroid, 29(1), 111-123. https://doi.org/10.1089/thy.2018.0349
Migaud, H., Davie, A. & Taylor, J. F. (2010). Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. Journal of fish biology, 76(1), 27-68. https://doi.org/10.1111/j.1095-8649.2009.02500.x
Mishra, I., Singh, D. & Kumar, V. (2017). Seasonal alterations in the daily rhythms in hypothalamic expression of genes involved in the photoperiodic transduction and neurosteroid-dependent processes in migratory blackheaded buntings. Journal of Neuroendocrinology, 29(5). https://doi.org/10.1111/jne.12469
Morris, K. M., Hindle, M. M., Boitard, S., Burt, D. W., Danner, A. F., Eory, L. & Smith, J. (2020). The quail genome: insights into social behaviour, seasonal biology and infectious disease response. BMC biology, 18(1), 1-18.
Nakane, Y., Ikegami, K., Iigo, M., Ono, H., Takeda, K., Takahashi, D. & Yoshimura, T. (2013). The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nature Communications, 4(1), 1–7. https://doi.org/10.1038/ncomms3108
Narsimhan, P. V. & Sundararaj, B. I. (1971). Effects of stress on carbohydrate metabolism in the teleost Notopterus notopterus (Pallas). Journal of Fish Biology, 3(4), 441–451. https://doi.org/10.1111/j.1095-8649.1971.tb05916.x
Narsimhan, P.V. (1970) Experimental studies on the carbohydrate metabolism in some freshwater teleostean fishes, Ph.D. thesis, University of Delhi, Delhi.
Nelson, E. R. & Habibi, H. R. (2016). Thyroid hormone regulates vitellogenin by inducing estrogen receptor alpha in the goldfish liver. Molecular and Cellular Endocrinology, 436, 259–267. https://doi.org/10.1016/j.mce.2016.08.045
Nelson, E. R., Allan, E. R. O., Pang, F. Y. & Habibi, H. R. (2010). Thyroid hormone and reproduction: Regulation of estrogen receptors in goldfish gonads. Molecular Reproduction and Development, 77(9), 784–794. https://doi.org/10.1002/mrd.21219
Nisembaum, L. G., Martin, P., Lecomte, F. & Falcón, J. (2021). Melatonin and osmoregulation in fish: A focus on Atlantic salmon Salmo salar smoltification. Journal of Neuroendocrinology, 33(3), e12955. https://doi.org/10.1111/jne.12955
Ohga, H., Ohta, K. & Matsuyama, M. (2023). Long-day stimulation increases thyroid-stimulating hormone expression and affects gonadal development in chub mackerel. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 275, 111334. https://doi.org/10.1016/j.cbpa.2022.111334
Pankhurst, N. W. & King, H. R. (2010). Temperature and salmonid reproduction: Implications for aquaculture. Journal of Fish Biology, 76(1), 69–85. https://doi.org/10.1111/j.1095-8649.2009.02484.x
Parkinson, T. J. & Follett, B. K. (1994). Effect of thyroidectomy upon seasonality in rams. Journal of Reproduction and Fertility, 101, 51–58. https://doi.org/10.1530/jrf.0.1010051
Pavlov, D. S., Pavlov, E. D., Kostin, V. V. & Ganzha, E. V. (2022). Influence of water temperature on thyroid hormones and on the movement behavior of juvenile rainbow trout (Oncorhynchus mykiss) in water flow. Environmental Biology of Fishes, 1-12. https://doi.org/10.1007/s10641-022-01336-3
Picard-Aitken, M., Fournier, H., Pariseau, R., Marcogliese, D. J. & Cyr, D. G. (2007). Thyroid disruption in walleye (Sander vitreus) exposed to environmental contaminants: Cloning and use of iodothyronine deiodinases as molecular biomarkers. Aquatic Toxicology, 83(3), 200–211. https://doi.org/10.1016/j.aquatox.2007.04.004
Polat, H., Ozturk, R. C., Terzi, Y., Aydin, I. & Kucuk, E. (2021). Effect of photoperiod manipulation on spawning time and performance of turbot (Scophthalmus maximus). Aquaculture Studies, 21(3), 109-115. DOI : 10.4194/2618-6381-v21_3_03
Provinciali, M., Muzzioli, M., DiStefano, G. & Fabris, N. (1991). Recovery of spleen cell natural killer activity by thyroid hormone treatment in old mice. Natural Immunity and Cell Growth Regulation, 10(4), 226–236.
Quesada-García, A., Valdehita, A., Kropf, C., Casanova-Nakayama, A., Segner, H. & Navas, J. M. (2014). Thyroid signaling in immune organs and cells of the teleost fish rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology, 38(1), 166–174. https://doi.org/10.1016/j.fsi.2014.03.016
Raimondo, S. (2012). Incorporating temperature-driven seasonal variation in survival, growth, and reproduction into population models for small fish. Marine Ecology Progress Series, 469, 101–112. https://doi.org/10.3354/meps09988
Russo, S. C., Salas-Lucia, F. & Bianco, A. C. (2021). Deiodinases and the metabolic code for thyroid hormone action. Endocrinology, 162(8), bqab059. https://doi.org/10.1210/endocr/bqab059
Sabatino, L., Kusmic, C. & Iervasi, G. (2020). Modification of cardiac thyroid hormone deiodinases expression in an ischemia/reperfusion rat model after T3 infusion. Molecular and Cellular Biochemistry, 475(1), 205-214. https://doi.org/10.1007/s11010-020-03873-w
Sáenz de Miera, C., Sage-Ciocca, D., Simonneaux, V., Pévet, P. & Monecke, S. (2018). Melatonin-independent photoperiodic entrainment of the circannual TSH rhythm in the pars tuberalis of the European hamster. Journal of Biological Rhythms, 33(3), 302-317. https://doi.org/10.1177/0748730418766601
Sciarrillo, R., Laforgia, V., Cavagnuolo, A., Varano, L. & Virgilio, F. (2009). Annual variations of thyroid activity in the lizard Podarcis sicula (squamata, lacertidae). Italian Journal of Zoology, 67(3), 263–267. https://doi.org/10.1080/11250000009356321
Seale, L. A., Gilman, C. L., Zavacki, A. M., Larsen, P. R., Inokuchi, M., Breves, J. P. & Seale, A. P. (2021). Regulation of thyroid hormones and branchial iodothyronine deiodinases during freshwater acclimation in tilapia. Molecular and Cellular Endocrinology, 538, 111450. https://doi.org/10.1016/j.mce.2021.111450
Shahjahan, M., Kitahashi, T., Ogawa, S. & Parhar, I. S. (2013). Temperature differentially regulates the two kisspeptin systems in the brain of zebrafish. General and Comparative Endocrinology, 193, 79–85. https://doi.org/10.1016/j.ygcen.2013.07.015
Shao, Y. T., Roufidou, C., Chung, P. C. & Borg, B. (2019). Changes in kisspeptin, GnRH, and gonadotropin mRNA levels in male Threespine stickleback (Gasterosteus aculeatus) during photoperiod-induced sexual maturation. Evolutionary Ecology Research, 20(3), 317-329.
Shi, Q., Sun, N., Kou, H., Wang, H. & Zhao, H. (2018). Chronic effects of mercury on Bufo gargarizans larvae: thyroid disruption, liver damage, oxidative stress and lipid metabolism disorder. Ecotoxicology and environmental safety, 164, 500-509. https://doi.org/10.1016/j.ecoenv.2018.08.058
Skoglund, H., Einum, S. & Robertsen, G. (2011). Competitive interactions shape offspring performance in relation to seasonal timing of emergence in Atlantic salmon. Journal of Animal Ecology, 80(2), 365–374. https://doi.org/10.1111/j.1365-2656.2010.01783.x
Stahl, A. & Seite, R. (1960). Contribution a letude du sac vasculaire des poissons teleosteens. Comptes rendus des seances de la societe de biologie et de ses filiales, 154(5), 1020–1022.
Sueiro, C., Carrera, I., Ferreiro, S., Molist, P., Adrio, F., Anadón, R. & Rodríguez-Moldes, I. (2007). New insights on saccus vasculosus evolution: A developmental and immunohistochemical study in elasmobranchs. Brain, Behavior and Evolution, 70(3), 187–204. https://doi.org/10.1159/000104309
Sundararaj, B. I. & Vasal, S. (1976). Photoperiod and Temperature Control in the Regulation of Reproduction in the Female Catfish Heteropneustes fossilis. Journal of the Fisheries Research Board of Canada, 33(4), 959–973. https://doi.org/10.1139/f76-123
Tian, F., Liu, S., Shi, J., Qi, H., Zhao, K. & Xie, B. (2019). Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii . BMC Genomics, 20(1), 1–13. https://doi.org/10.1186/s12864-018-5358-6
Tovo-Neto, A., da Silva Rodrigues, M., Habibi, H. R. & Nóbrega, R. H. (2018). Thyroid hormone actions on male reproductive system of teleost fish. General and Comparative Endocrinology, 265, 230-236. https://doi.org/10.1016/j.ygcen.2018.04.023
Trivedi, A. K., Sur, S., Sharma, A., Taufique, S. T., Gupta, N. J. & Kumar, V. (2019). Temperature alters the hypothalamic transcription of photoperiod responsive genes in induction of seasonal response in migratory redheaded buntings. Molecular and Cellular Endocrinology, 493, 110454. https://doi.org/10.1016/j.mce.2019.110454
Van der Geyten, S., Byamungu, N., Reyns, G. E., Kühn, E. R. & Darras, V. M. (2005). Iodothyronine deiodinases and the control of plasma and tissue thyroid hormone levels in hyperthyroid tilapia (Oreochromis niloticus). Journal of Endocrinology, 184(3), 467–479. https://doi.org/10.1677/joe.1.05986
Van Der Geyten, S., Mol, K. A., Pluymers, W., Kühn, E. R. & Darras, V. M. (1998). Changes in plasma T3 during fasting/refeeding in tilapia (Oreochromis niloticus) are mainly regulated through changes in hepatic type II iodothyronine deiodinase. Fish Physiology and Biochemistry, 19(2), 135–143. https://doi.org/10.1023/A:1007790527748
Verma, R. & Haldar, C. (2019). Expression of receptors for melatonin (MT1), thyroid hormone (TR-α), deiodinase (Dio-2), glucose transporters (GLUT-1 &4) and its relation with splenic cell survival (Bcl-2) of golden hamster, Mesocricetus auratus. Biological Rhythm Research, 50(3), 454-465. https://doi.org/10.1080/09291016.2018.1464632
Walpita, C. N., Grommen, S. V. H., Darras, V. M. & Van der Geyten, S. (2007). The influence of stress on thyroid hormone production and peripheral deiodination in the Nile tilapia (Oreochromis niloticus). General and Comparative Endocrinology, 150(1), 18–25. https://doi.org/10.1016/j.ygcen.2006.07.002
Wambiji, N., Park, Y. J., Kim, S. J., Hur, S. P., Takeuchi, Y. & Takemura, A. (2011a). Expression of type II iodothyronine deiodinase gene in the brain of a tropical spinefoot, Siganus guttatus. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, 160(4), 447–452. https://doi.org/10.1016/j.cbpa.2011.03.023
Wambiji, N., Park, Y. J., Park, J. G., Kim, S. J., Hur, S. P., Takeuchi, Y. & Takemura, A. (2011b). Expression patterns of type II and III iodothyronine deiodinase genes in the liver of the goldlined spinefoot, Siganus guttatus. Fisheries Science, 77(3), 301–311. https://doi.org/10.1007/s12562-011-0330-2
Watanabe, M., Yasuo, S., Watanabe, T., Yamamura, T., Nakao, N., Ebihara, S. & Yoshimura, T. (2004). Photoperiodic regulation of type 2 deiodinase gene in djungarian hamster: Possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology, 145(4), 1546–1549. https://doi.org/10.1210/en.2003-1593
Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K. & Ebihara, S. (2003). Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature, 426(6963), 178–181. https://doi.org/10.1038/nature02117
Zhang, D., Xiong, H., Mennigen, J. A., Popesku, J. T., Marlatt, V. L., Martyniuk, C. J., Crump, K., Cossins, A. R., Xia, X. & Trudeau, V. L. (2009). Defining global neuroendocrine gene expression patterns associated with reproductive seasonality in fish. PLoS ONE, 4(6). https://doi.org/10.1371/journal.pone.0005816
Chang, J., Hao, W., Xu, Y., Xu, P., Li, W., Li, J. & Wang, H. (2018). Stereoselective degradation and thyroid endocrine disruption of lambda-cyhalothrin in lizards (Eremias argus) following oral exposure. Environmental Pollution, 232, 300-309. https://doi.org/10.1016/j.envpol.2017.09.072
Chaube, R. & Joy, K. P. (2002). Effects of altered photoperiod and temperature, serotonin-affecting drugs, and melatonin on brain tyrosine hydroxylase activity in female catfish, Heteropneustes fossilis: A study correlating ovarian activity changes. Journal of Experimental Zoology, 293(6), 585–593.https://doi.org/10.1002/jez.10185
Chaube, R., Sharma, S., Senthilkumaran, B., Bhat, S. G. & Joy, K. P. (2020). Expression profile of kisspeptin2 and gonadotropin-releasing hormone2 mRNA during photo-thermal and melatonin treatments in the female air-breathing catfish Heteropneustes fossilis. Fish Physiology and Biochemistry, 46(6), 2403-2419. https://doi.org/10.10 07/s10695-020-00888-4
Chaube, R., Sharma, S., Senthilkumaran, B., Bhat, S. G. & Joy, K. P. (2022). Kisspeptins stimulate the hypothalamus-pituitary-ovarian axis and induce final oocyte maturation and ovulation in female stinging catfish (Heteropneustes fossilis): Evidence from in vivo and in vitro studies. Aquaculture, 548, 737734. https://doi.org/10.1 016/j.aquaculture.2021.737734
Chi, L., Li, X., Liu, Q. & Liu, Y. (2017). Photoperiod regulate gonad development via kisspeptin/kissr in hypothalamus and saccus vasculosus of Atlantic salmon (Salmo salar). PloS one, 12(2), e0169569. https://doi.org/10.1371/journal.pone.01 69569
Chi, L., Li, X., Liu, Q. & Liu, Y. (2019). Photoperiod may regulate growth via leptin receptor A1 in the hypothalamus and saccus vasculosus of Atlantic salmon (Salmo salar). Animal Cells and Systems, 23(3), 200-208. . https://doi.org/10.10 80/19768354.2019.1595138
Chomczynski, P. & Sacchi, N. (2006). The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on. Nature Protocols, 1(2), 581–585.https://doi.org/10.1038/nprot.2006.83
Cyr, D. G. & Eales, J. G. (1988). Influence of thyroidal status on ovarian function in rainbow trout, Salmo gairdneri. Journal of Experimental Zoology, 248(1), 81–87. https://doi.org/10.1002/jez.140248 0110
Cyr, D. G., Idler, D. R., Audet, C., McLeese, J. M. & Eales, J. G. (1998). Effects of long-term temperature acclimation on thyroid hormone deiodinase function, plasma thyroid hormone levels, growth, and reproductive status of male atlantic cod, Gadus morhua. General and Comparative Endocrinology, 109(1), 24–36.https://doi.org/10.1006/gcen.19 97.6994
Deal, C. K. & Volkoff, H. (2021). Response of the thyroid axis and appetite-regulating peptides to fasting and overfeeding in goldfish (Carassius auratus). Molecular and Cellular Endocrinology, 528, 111229. https://doi.org/10.1016/j.mce.20 21.11122 9
Doyle, A., Cowan, M. E., Migaud, H., Wright, P. J. & Davie, A. (2021). Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 260, 111000. https://doi.org/10.1016/j.cbpa.2021.111000
Eales, J. G. & Brown, S. B. (1993). Measurement and regulation of thyroidal status in teleost fish. Reviews in Fish Biology and Fisheries, 3(4), 299–347. https://doi.org/10.1007/BF00043383
Eales, J. G. (2019). The relationship between ingested thyroid hormones, thyroid homeostasis and iodine metabolism in humans and teleost fish. General and Comparative Endocrinology, 280, 62-72. https://doi.org/10.1016/j.ygcen.2019.04.012
Falcon, J., Migaud, H., Muñoz-Cueto, J. A. & Carrillo, M. (2010). Current knowledge on the melatonin system in teleost fish. General and Comparative Endocrinology, 165(3), 469–482. https://doi.org/10.1016/j.ygcen.2009.04.026
Feng, N. Y., Marchaterre, M. A. & Bass, A. H. (2019). Melatonin receptor expression in vocal, auditory, and neuroendocrine centers of a highly vocal fish, the plainfin midshipman (Porichthys notatus). Journal of Comparative Neurology, 527(8), 1362-1377. https://doi.org/10.1002/cne.24629
Fleming, M. S., Maugars, G., Lafont, A. G., Rancon, J., Fontaine, R., Nourizadeh-Lillabadi, R., Weltzien, F. A., Yebra-Pimentel, E. S., Dirks, R., McCormick, S. D., Rousseau, K., Martin, P. & Dufour, S. (2019). Functional divergence of thyrotropin beta-subunit paralogs gives new insights into salmon smoltification metamorphosis. Scientific Reports, 9(1), 1–15. https://doi.org/10.1038/s41598-019-40019-5
Fournie, J. W., Wolfe, M. J., Wolf, J. C., Courtney, L. A., Johnson, R. D. & Hawkins, W. E. (2005). Diagnostic criteria for proliferative thyroid lesions in bony fishes. Toxicologic Pathology, 33(5), 540–551. https://doi.org/10.1080/01926230500214509
Galton, V. A. (1992). Thyroid hormone receptors and iodothyronine deiodinases in the developing Mexican axolotl, Ambystoma mexicanum. General and Comparative Endocrinology, 85(1), 62–70. https://doi.org/10.1016/0016-6480(92)90172-G
Garcia, I., Garcia de Souza, J., Plaul, S. E., Miranda, L. & Colautti, D. (2022). Effect of photoperiod and temperature on ovarian maturation in the small characid fish Cheirodon interruptus. Journal of Applied Aquaculture, 1-13. https://doi.org/10.10 80/10454438.2022.2047867
Germain, D. L. S. & Galton, V. A. (1997). The deiodinase family of selenoproteins. Thyroid, 7(4), 655-668. https://doi.org/10.1089/thy.1997.7.655
Goto-Kazeto, R., Kazeto, Y. & Trant, J. M. (2003). Cloning and seasonal changes in ovarian expression of a TSH receptor in the channel catfish, Ictalurus punctatus. Fish Physiology and Biochemistry, 28(1), 339-340. https://doi.org/10.1023/B:FISH.0000030578.25321.8f
Guh, Y. J., Tamai, T. K. & Yoshimura, T. (2019). The underlying mechanisms of vertebrate seasonal reproduction. Proceedings of the Japan Academy, Series B, 95(7), 343-357. https://doi.org/10.2183/pjab.95.025
Hafeez, M. & Ahmad, I. (2021). Melatonin and Seasonal Reproduction in Teleosts. In Recent updates in molecular Endocrinology and Reproductive Physiology of Fish (pp. 181-192). Springer, Singapore. https://doi.org/10.1007/978-981-15-8369-8_13
Hsu, S. Y., Liang, S. G. & Hsueh, A. J. (1998). Characterization of two LGR genes homologous to gonadotropin and thyrotropin receptors with extracellular leucine-rich repeats and a G protein-coupled, seven-transmembrane region. Molecular endocrinology, 12(12), 1830-1845. https://doi.org/10.1210/mend.12.12.0211
Hughes, T. E. & McNABB, F. M. A. (1986). Avian hepatic T-3 production by two pathways of 5′-monodeiodination: Effects of fasting and patterns during development. 238:393-399. https://doi.org/10.1002/jez.1402380312
Hur, S. P., Mahardini, A., Takeuchi, Y., Imamura, S., Wambiji, N., Rizky, D. & Takemura, A. (2020). Expression profiles of types 2 and 3 iodothyronine deiodinase genes in relation to vitellogenesis in a tropical damselfish, Chrysiptera cyanea. General and Comparative Endocrinology, 285, 113264. https://doi.org/10.1016/j.ygcen.2019.113264
Husse, J., Eichele, G. & Oster, H. (2015). Synchronization of the mammalian circadian timing system: Light can control peripheral clocks independently of the SCN clock: Alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time. Bioessays, 37(10), 1119–1128. https://doi.org/10.1002/bies.20 1500026
Ikegami, K., Liao, X. H., Hoshino, Y., Ono, H., Ota, W., Ito, Y., Nishiwaki-Ohkawa, T., Sato, C., Kitajima, K., Iigo, M., Shigeyoshi, Y., Yamada, M., Murata, Y., Refetoff, S. & Yoshimura, T. (2014). Tissue-specific posttranslational modification allows functional targeting of thyrotropin. Cell Reports, 9(3), 801–809. https://doi.org/10.1016/j.celrep.201 4.10.0 06
Irachi, S., Hall, D. J., Fleming, M. S., Maugars, G., Dufour, S., Uchida, K. & Mccormick, S. D. (2021). Photoperiodic regulation of pituitary thyroid-stimulating hormone and brain deiodinase in Atlantic salmon. Molecular and Cellular Endocrinology, 519. https://doi.org/10.1016/j.mce.2020.111056
Köhrle, J. & Frädrich, C. (2022). Deiodinases control local cellular and systemic thyroid hormone availability. Free Radical Biology and Medicine. https://doi.org/10.1016/j.freeradbiomed.202 2.09.024
Kohrle, J. (1999). Local activation and inactivation of thyroid hormones: The deiodinase family. Molecular and Cellular Endocrinology, 151(1–2), 103–119. https://doi.org/10.1016/S0303-7207(99)00040-4
Köhrle, J. (2000). The deiodinase family: Selenoenzymes regulating thyroid hormone availability and action. Cellular and Molecular Life Sciences, 57(13–14), 1853–1863. https://doi.org/10.1007/PL00000667
Kupprat, F., Hölker, F. & Kloas, W. (2020). Can skyglow reduce nocturnal melatonin concentrations in Eurasian perch? Environmental Pollution, 262, 114324. https://doi.org/10.1016/j.envpol.2020.11 4324
Kwonm, J. Y., Chang, Y. J., Sohn, Y. C. & Aida, K. (1999). Plasma and ovarian thyroxine levels in relation to sexual maturation and gestation in female Sebastes inermis. Journal of Fish Biology, 54(2), 370–379. . https://doi.org/10.1111/j.1095-8649.1999.tb00836.x
Lalli, E. & Sassone-Corsi, P. (1995). Thyroid-stimulating hormone (TSH)-directed induction of the CREM gene in the thyroid gland participates in the long-term desensitization of the TSH receptor. Proceedings of the National Academy of Sciences of the United States of America, 92(21), 9633–9637. https://doi.org/10.1073/pnas.92.21.9633
Laslo, M., Denver, R. J. and Hanken, J. (2019). Evolutionary conservation of thyroid hormone receptor and deiodinase expression dynamics in ovo in a direct-developing frog, Eleutherodactylus coqui. Frontiers in endocrinology, 10, 307. https://doi.org/10.3389/fendo.2019.00307
Leiner, K. A., Han, G. S. & MacKenzie, D. S. (2000). The effects of photoperiod and feeding on the diurnal rhythm of circulating thyroid hormones in the red drum, Sciaenops ocellatus. General and Comparative Endocrinology, 120(1), 88–98. https://doi.org/10.1006/gcen.2000.7539
Lepine, M. & Verreault, J. (2022). Biotransformation of Dec-604 and potential effect on thyroid deiodinase activity in highly flame retardant-exposed gulls. Environmental Research, 215, 114268. https://doi.org/10.1016/j.envres.2022.1 14268
Li, Z. H., Li, P. & Wu, Y. (2021). Effects of temperature fluctuation on endocrine disturbance of grass carp Ctenopharyngodon idella under mercury chloride stress. Chemosphere, 263,128137.https://doi.org/10.1016/j.chemosphere.2020.128137
Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.20 01.1262
Lorgen, M., Casadei, E., Król, E., Douglas, A., Birnie, M. J., Ebbesson, L. O. E., Nilsen, T. O., Jordan, W. C., Jørgensen, E. H., Dardente, H., Hazlerigg, D. G. & Martin A.m, S. (2015). Functional divergence of type 2 deiodinase paralogs in the Atlantic salmon. Current Biology, 25(7), 936–941. https://doi.org/10.1016/j.cub.2015.01.074
Luongo, C., Dentice, M. & Salvatore, D. (2019). Deiodinases and their intricate role in thyroid hormone homeostasis. Nature Reviews Endocrinology, 15(8), 479-488.
Ma, Y., Ladisa, C., Chang, J. P. & Habibi, H. R. (2020). Seasonal related multifactorial control of pituitary gonadotropin and growth hormone in female goldfish: Influences of neuropeptides and thyroid hormone. Frontiers in endocrinology, 11, 175. https://doi.org/10.3389/fendo.2020.00175
MacLatchy, D. L. & Eales, J. G. (1992). Properties of T4 5′-deiodinating systems in various tissues of the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology, 86(2), 313–322. https://doi.org/10.1016/0016-6480(92)90116-2
MacLatchy, D. L., Kawauchi, H. & Eales, J. G. (1992). Stimulation of hepatic thyroxine 5’-deiodinase activity in rainbow trout (Oncorhynchus mykiss) by Pacific salmon growth hormone.., 101(4), 689–691. https://doi.org/10.1016/0300-9629(92)90344-p
Maeda, R., Shimo, T., Nakane, Y., Nakao, N. & Yoshimura, T. (2015). Ontogeny of the saccus vasculosus, a seasonal sensor in fish. Endocrinology, 156(11), 4238-4243. https://doi.org/10.1210/en.2015-1415
Mahardini, A., Rizky, D., Byun, J. H., Yamauchi, C., Takeuchi, Y. & Takemura, A. (2020). Food availability alters expression profiles of genes in relation to reproduction and nutrition in the females of tropical damselfish (Chrysiptera cyanea). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 333(9), 619-628. https://doi.org/10.1002/jez.2409
Marcinkowski, P., Hoyer, I., Specker, E., Furkert, J., Rutz, C., Neuenschwander, M. & Krause, G. (2019). A new highly thyrotropin receptor-selective small-molecule antagonist with potential for the treatment of Graves' orbitopathy. Thyroid, 29(1), 111-123. https://doi.org/10.1089/thy.2018.0349
Migaud, H., Davie, A. & Taylor, J. F. (2010). Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. Journal of fish biology, 76(1), 27-68. https://doi.org/10.1111/j.1095-8649.2009.02500.x
Mishra, I., Singh, D. & Kumar, V. (2017). Seasonal alterations in the daily rhythms in hypothalamic expression of genes involved in the photoperiodic transduction and neurosteroid-dependent processes in migratory blackheaded buntings. Journal of Neuroendocrinology, 29(5). https://doi.org/10.1111/jne.12469
Morris, K. M., Hindle, M. M., Boitard, S., Burt, D. W., Danner, A. F., Eory, L. & Smith, J. (2020). The quail genome: insights into social behaviour, seasonal biology and infectious disease response. BMC biology, 18(1), 1-18.
Nakane, Y., Ikegami, K., Iigo, M., Ono, H., Takeda, K., Takahashi, D. & Yoshimura, T. (2013). The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nature Communications, 4(1), 1–7. https://doi.org/10.1038/ncomms3108
Narsimhan, P. V. & Sundararaj, B. I. (1971). Effects of stress on carbohydrate metabolism in the teleost Notopterus notopterus (Pallas). Journal of Fish Biology, 3(4), 441–451. https://doi.org/10.1111/j.1095-8649.1971.tb05916.x
Narsimhan, P.V. (1970) Experimental studies on the carbohydrate metabolism in some freshwater teleostean fishes, Ph.D. thesis, University of Delhi, Delhi.
Nelson, E. R. & Habibi, H. R. (2016). Thyroid hormone regulates vitellogenin by inducing estrogen receptor alpha in the goldfish liver. Molecular and Cellular Endocrinology, 436, 259–267. https://doi.org/10.1016/j.mce.2016.08.045
Nelson, E. R., Allan, E. R. O., Pang, F. Y. & Habibi, H. R. (2010). Thyroid hormone and reproduction: Regulation of estrogen receptors in goldfish gonads. Molecular Reproduction and Development, 77(9), 784–794. https://doi.org/10.1002/mrd.21219
Nisembaum, L. G., Martin, P., Lecomte, F. & Falcón, J. (2021). Melatonin and osmoregulation in fish: A focus on Atlantic salmon Salmo salar smoltification. Journal of Neuroendocrinology, 33(3), e12955. https://doi.org/10.1111/jne.12955
Ohga, H., Ohta, K. & Matsuyama, M. (2023). Long-day stimulation increases thyroid-stimulating hormone expression and affects gonadal development in chub mackerel. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 275, 111334. https://doi.org/10.1016/j.cbpa.2022.111334
Pankhurst, N. W. & King, H. R. (2010). Temperature and salmonid reproduction: Implications for aquaculture. Journal of Fish Biology, 76(1), 69–85. https://doi.org/10.1111/j.1095-8649.2009.02484.x
Parkinson, T. J. & Follett, B. K. (1994). Effect of thyroidectomy upon seasonality in rams. Journal of Reproduction and Fertility, 101, 51–58. https://doi.org/10.1530/jrf.0.1010051
Pavlov, D. S., Pavlov, E. D., Kostin, V. V. & Ganzha, E. V. (2022). Influence of water temperature on thyroid hormones and on the movement behavior of juvenile rainbow trout (Oncorhynchus mykiss) in water flow. Environmental Biology of Fishes, 1-12. https://doi.org/10.1007/s10641-022-01336-3
Picard-Aitken, M., Fournier, H., Pariseau, R., Marcogliese, D. J. & Cyr, D. G. (2007). Thyroid disruption in walleye (Sander vitreus) exposed to environmental contaminants: Cloning and use of iodothyronine deiodinases as molecular biomarkers. Aquatic Toxicology, 83(3), 200–211. https://doi.org/10.1016/j.aquatox.2007.04.004
Polat, H., Ozturk, R. C., Terzi, Y., Aydin, I. & Kucuk, E. (2021). Effect of photoperiod manipulation on spawning time and performance of turbot (Scophthalmus maximus). Aquaculture Studies, 21(3), 109-115. DOI : 10.4194/2618-6381-v21_3_03
Provinciali, M., Muzzioli, M., DiStefano, G. & Fabris, N. (1991). Recovery of spleen cell natural killer activity by thyroid hormone treatment in old mice. Natural Immunity and Cell Growth Regulation, 10(4), 226–236.
Quesada-García, A., Valdehita, A., Kropf, C., Casanova-Nakayama, A., Segner, H. & Navas, J. M. (2014). Thyroid signaling in immune organs and cells of the teleost fish rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology, 38(1), 166–174. https://doi.org/10.1016/j.fsi.2014.03.016
Raimondo, S. (2012). Incorporating temperature-driven seasonal variation in survival, growth, and reproduction into population models for small fish. Marine Ecology Progress Series, 469, 101–112. https://doi.org/10.3354/meps09988
Russo, S. C., Salas-Lucia, F. & Bianco, A. C. (2021). Deiodinases and the metabolic code for thyroid hormone action. Endocrinology, 162(8), bqab059. https://doi.org/10.1210/endocr/bqab059
Sabatino, L., Kusmic, C. & Iervasi, G. (2020). Modification of cardiac thyroid hormone deiodinases expression in an ischemia/reperfusion rat model after T3 infusion. Molecular and Cellular Biochemistry, 475(1), 205-214. https://doi.org/10.1007/s11010-020-03873-w
Sáenz de Miera, C., Sage-Ciocca, D., Simonneaux, V., Pévet, P. & Monecke, S. (2018). Melatonin-independent photoperiodic entrainment of the circannual TSH rhythm in the pars tuberalis of the European hamster. Journal of Biological Rhythms, 33(3), 302-317. https://doi.org/10.1177/0748730418766601
Sciarrillo, R., Laforgia, V., Cavagnuolo, A., Varano, L. & Virgilio, F. (2009). Annual variations of thyroid activity in the lizard Podarcis sicula (squamata, lacertidae). Italian Journal of Zoology, 67(3), 263–267. https://doi.org/10.1080/11250000009356321
Seale, L. A., Gilman, C. L., Zavacki, A. M., Larsen, P. R., Inokuchi, M., Breves, J. P. & Seale, A. P. (2021). Regulation of thyroid hormones and branchial iodothyronine deiodinases during freshwater acclimation in tilapia. Molecular and Cellular Endocrinology, 538, 111450. https://doi.org/10.1016/j.mce.2021.111450
Shahjahan, M., Kitahashi, T., Ogawa, S. & Parhar, I. S. (2013). Temperature differentially regulates the two kisspeptin systems in the brain of zebrafish. General and Comparative Endocrinology, 193, 79–85. https://doi.org/10.1016/j.ygcen.2013.07.015
Shao, Y. T., Roufidou, C., Chung, P. C. & Borg, B. (2019). Changes in kisspeptin, GnRH, and gonadotropin mRNA levels in male Threespine stickleback (Gasterosteus aculeatus) during photoperiod-induced sexual maturation. Evolutionary Ecology Research, 20(3), 317-329.
Shi, Q., Sun, N., Kou, H., Wang, H. & Zhao, H. (2018). Chronic effects of mercury on Bufo gargarizans larvae: thyroid disruption, liver damage, oxidative stress and lipid metabolism disorder. Ecotoxicology and environmental safety, 164, 500-509. https://doi.org/10.1016/j.ecoenv.2018.08.058
Skoglund, H., Einum, S. & Robertsen, G. (2011). Competitive interactions shape offspring performance in relation to seasonal timing of emergence in Atlantic salmon. Journal of Animal Ecology, 80(2), 365–374. https://doi.org/10.1111/j.1365-2656.2010.01783.x
Stahl, A. & Seite, R. (1960). Contribution a letude du sac vasculaire des poissons teleosteens. Comptes rendus des seances de la societe de biologie et de ses filiales, 154(5), 1020–1022.
Sueiro, C., Carrera, I., Ferreiro, S., Molist, P., Adrio, F., Anadón, R. & Rodríguez-Moldes, I. (2007). New insights on saccus vasculosus evolution: A developmental and immunohistochemical study in elasmobranchs. Brain, Behavior and Evolution, 70(3), 187–204. https://doi.org/10.1159/000104309
Sundararaj, B. I. & Vasal, S. (1976). Photoperiod and Temperature Control in the Regulation of Reproduction in the Female Catfish Heteropneustes fossilis. Journal of the Fisheries Research Board of Canada, 33(4), 959–973. https://doi.org/10.1139/f76-123
Tian, F., Liu, S., Shi, J., Qi, H., Zhao, K. & Xie, B. (2019). Transcriptomic profiling reveals molecular regulation of seasonal reproduction in Tibetan highland fish, Gymnocypris przewalskii . BMC Genomics, 20(1), 1–13. https://doi.org/10.1186/s12864-018-5358-6
Tovo-Neto, A., da Silva Rodrigues, M., Habibi, H. R. & Nóbrega, R. H. (2018). Thyroid hormone actions on male reproductive system of teleost fish. General and Comparative Endocrinology, 265, 230-236. https://doi.org/10.1016/j.ygcen.2018.04.023
Trivedi, A. K., Sur, S., Sharma, A., Taufique, S. T., Gupta, N. J. & Kumar, V. (2019). Temperature alters the hypothalamic transcription of photoperiod responsive genes in induction of seasonal response in migratory redheaded buntings. Molecular and Cellular Endocrinology, 493, 110454. https://doi.org/10.1016/j.mce.2019.110454
Van der Geyten, S., Byamungu, N., Reyns, G. E., Kühn, E. R. & Darras, V. M. (2005). Iodothyronine deiodinases and the control of plasma and tissue thyroid hormone levels in hyperthyroid tilapia (Oreochromis niloticus). Journal of Endocrinology, 184(3), 467–479. https://doi.org/10.1677/joe.1.05986
Van Der Geyten, S., Mol, K. A., Pluymers, W., Kühn, E. R. & Darras, V. M. (1998). Changes in plasma T3 during fasting/refeeding in tilapia (Oreochromis niloticus) are mainly regulated through changes in hepatic type II iodothyronine deiodinase. Fish Physiology and Biochemistry, 19(2), 135–143. https://doi.org/10.1023/A:1007790527748
Verma, R. & Haldar, C. (2019). Expression of receptors for melatonin (MT1), thyroid hormone (TR-α), deiodinase (Dio-2), glucose transporters (GLUT-1 &4) and its relation with splenic cell survival (Bcl-2) of golden hamster, Mesocricetus auratus. Biological Rhythm Research, 50(3), 454-465. https://doi.org/10.1080/09291016.2018.1464632
Walpita, C. N., Grommen, S. V. H., Darras, V. M. & Van der Geyten, S. (2007). The influence of stress on thyroid hormone production and peripheral deiodination in the Nile tilapia (Oreochromis niloticus). General and Comparative Endocrinology, 150(1), 18–25. https://doi.org/10.1016/j.ygcen.2006.07.002
Wambiji, N., Park, Y. J., Kim, S. J., Hur, S. P., Takeuchi, Y. & Takemura, A. (2011a). Expression of type II iodothyronine deiodinase gene in the brain of a tropical spinefoot, Siganus guttatus. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, 160(4), 447–452. https://doi.org/10.1016/j.cbpa.2011.03.023
Wambiji, N., Park, Y. J., Park, J. G., Kim, S. J., Hur, S. P., Takeuchi, Y. & Takemura, A. (2011b). Expression patterns of type II and III iodothyronine deiodinase genes in the liver of the goldlined spinefoot, Siganus guttatus. Fisheries Science, 77(3), 301–311. https://doi.org/10.1007/s12562-011-0330-2
Watanabe, M., Yasuo, S., Watanabe, T., Yamamura, T., Nakao, N., Ebihara, S. & Yoshimura, T. (2004). Photoperiodic regulation of type 2 deiodinase gene in djungarian hamster: Possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology, 145(4), 1546–1549. https://doi.org/10.1210/en.2003-1593
Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K. & Ebihara, S. (2003). Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature, 426(6963), 178–181. https://doi.org/10.1038/nature02117
Zhang, D., Xiong, H., Mennigen, J. A., Popesku, J. T., Marlatt, V. L., Martyniuk, C. J., Crump, K., Cossins, A. R., Xia, X. & Trudeau, V. L. (2009). Defining global neuroendocrine gene expression patterns associated with reproductive seasonality in fish. PLoS ONE, 4(6). https://doi.org/10.1371/journal.pone.0005816
Issue
Section
Research Articles
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
This work is licensed under Attribution-NonCommercial 4.0 International (CC BY-NC 4.0) © Author (s)
How to Cite
Temporal expression of thyroid hormone regulating genes (tsh-b, tsh-r, dio2 and dio3) and their correlation with annual reproductive cycle of the Indian freshwater catfish, Heteropneustes fossilis (Bloch). (2023). Journal of Applied and Natural Science, 15(1), 41-56. https://doi.org/10.31018/jans.v15i1.4179
