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Abstract
Thyroid hormones are known to regulate the basal metabolism rate of an organism. They are also known to regulate the seasonal reproduction of long-day breeding vertebrates in response to thyrotropin induced deiodinase enzymes switching in the brain. The current study attempted to investigate the effect of intraperitoneal administration of thyroxine (T4) and tri-iodothyronine (T3) hormones at various doses on gonadal recrudescence, plasma estradiol-17β and quantitative expression analysis of genes encoding for gonadotropin, thyrotropin, and deiodinases. The estradiol-17β levels were not affected by either thyroid hormone; however, the gonado-somatic index (GSI) and ovarian histology were varying. The gonadotropin releasing hormone 2 (gnrh2) and follicle stimulating hormone-β subunit (fsh-b) gene expressions correspond to the fish GSI and ovarian histology. The gene expressions show that T4 inhibits the expression of thyroid stimulating hormone-β subunit (tsh-b) and type 3 deiodinase (dio3), though it enhances the expression of type 2 deiodinase (dio2). T3, on the other hand, inhibits tsh-b and dio2 expression while increasing dio3 expression. In summary, the T4 appears to regulate gonadal recrudescence in Heteropneustes fossilis in a dose-dependent manner, whereas the T3 appears to have no effect on gonadal activity.
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References
- Allan, E. R., & Habibi, H. R. (2012). Direct effects of triiodothyronine on production of anterior pituitary hormones and gonadal steroids in goldfish. Molecular Reproduction and Development, 79(9), 592-602. DOI: https://doi.org/10.1002/mrd.22066
- Biswas, A. K., Seoka, M., Tanaka, Y., Takii, K., & Kumai, H. (2006). Effect of photoperiod manipulation on the growth performance and stress response of juvenile red sea bream (Pagrus major). Aquaculture, 258(1-4), 350-356. DOI: https://doi.org/10.1016/j.aquaculture.2006.03.048
- Coimbra, A. M., Reis-Henriques, M. A., & Darras, V. M. (2005). Circulating thyroid hormone levels and iodothyronine deiodinase activities in Nile tilapia (Oreochromis niloticus) following dietary exposure to Endosulfan and Aroclor 1254. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 141(1), 8-14. DOI: https://doi.org/10.1016/j.cca.2005.04.006
- Cyr, D. G., & Eales, J. G. (1996). Interrelationships between thyroidal and reproductive endocrine systems in fish. Reviews in Fish Biology and Fisheries, 6(2), 165-200. DOI: https://doi.org/10.1007/BF00182342
- Flood, D. E., Fernandino, J. I., & Langlois, V. S. (2013). Thyroid hormones in male reproductive development: evidence for direct crosstalk between the androgen and thyroid hormone axes. General and comparative endocrinology, 192, 2-14. DOI: https://doi.org/10.1016/j.ygcen.2013.02.038
- Furlow, J. D., & Neff, E. S. (2006). A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends in Endocrinology & Metabolism, 17(2), 40-47. DOI: https://doi.org/10.1016/j.tem.2006.01.007
- Gereben, B., Zavacki, A. M., Ribich, S., Kim, B. W., Huang, S. A., Simonides, W. S., .Bianco, A. C. (2008). Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocrine reviews, 29(7), 898-938. DOI: https://doi.org/10.1210/er.2008-0019
- Hernandez, A., Quignodon, L., Martinez, M. E., Flamant, F., & St. Germain, D. L. (2010). Type 3 deiodinase deficiency causes spatial and temporal alterations in brain T3 signaling that are dissociated from serum thyroid hormone levels. Endocrinology, 151(11), 5550-5558. DOI: https://doi.org/10.1210/en.2010-0450
- 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. DOI: https://doi.org/10.1016/j.ygcen.2019.113264
- Hurlburt, M. E. (1977). Role of the thyroid gland in ovarian maturation of the goldfish, Carassius auratus L. Canadian journal of zoology, 55(11), 1906-1913. DOI: https://doi.org/10.1139/z77-244
- Kumari, P., Kumar, M., Sehgal, N., & Aggarwal, N. (2020). In silico analysis of kiss2, expression studies and protein–protein interaction with gonadotropin-releasing hormone 2 (GnRH2) and luteinizing hormone beta (LHβ) in Heteropneustes fossilis. Journal of Biomolecular Structure and Dynamics, 1-15. DOI: https://doi.org/10.1080/07391102.2020.1860820
- Larsen, D. A., Dickey, J. T., & Dickhoff, W. W. (1997). Quantification of salmon α-and thyrotropin (TSH) β-subunit messenger RNA by an RNase protection assay: Regulation by thyroid hormones. General and Comparative Endocrinology, 107(1), 98-108. DOI: https://doi.org/10.1006/gcen.1997.6900
- Leatherland, J. F., Lin, L., Down, N. E., & Donaldson, E. M. (1989). Thyroid hormone content of eggs and early developmental stages of five Oncorhynchus species. Canadian Journal of Fisheries and Aquatic Sciences, 46(12), 2140-2145. DOI: https://doi.org/10.1139/f89-264
- 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. DOI: https://doi.org/10.3389/fendo.2020.00175
- Morais, R. D. V. S., Nóbrega, R. H., Gómez-González, N. E., Schmidt, R., Bogerd, J., França, L. R., & Schulz, R. W. (2013). Thyroid hormone stimulates the proliferation of Sertoli cells and single type A spermatogonia in adult zebrafish (Danio rerio) testis. Endocrinology, 154(11), 4365-4376. DOI: https://doi.org/10.1210/en.2013-1308
- 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. DOI: https://doi.org/10.1016/j.mce.2016.08.045
- Norberg, B., Brown, C. L., Halldorsson, O., Stensland, K., & Björnsson, B. T. (2004). Photoperiod regulates the timing of sexual maturation, spawning, sex steroid and thyroid hormone profiles in the Atlantic cod (Gadus morhua). Aquaculture, 229(1-4), 451-467. DOI: https://doi.org/10.1016/S0044-8486(03)00393-4
- Pant, D. R., Ila, K., Sahu, U.B., & Sehgal, N. (2023). 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). Journal of Applied and Natural Science, 15(1).
- Power, D. M., Llewellyn, L., Faustino, M., Nowell, M. A., Björnsson, B. T., Einarsdóttir, I. E., & Sweeney, G. E. (2001). Thyroid hormones in growth and development of fish. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 130(4), 447-459. DOI: https://doi.org/10.1016/S1532-0456(01)00271-X
- 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. DOI: https://doi.org/10.1007/s11010-020-03873-w
- Sehgal, A., & Sundararaj, B. I. (1970). Effects of various photoperiodic regimens on the ovary of the catfish, Heteropneustes fossilis (Bloch) during the spawning and the postspawning periods. Biology of Reproduction, 2(3), 425-434. DOI: https://doi.org/10.1095/biolreprod2.3.425
- Sohn, Y. C., Yoshiura, Y., Kobayashi, M., & Aida, K. (1999). Seasonal changes in mRNA levels of gonadotropin and thyrotropin subunits in the goldfish, Carassius auratus. General and comparative endocrinology, 113(3), 436-444. DOI: https://doi.org/10.1006/gcen.1998.7224
- Swapna, I., Rajasekhar, M., Supriya, A., Raghuveer, K., Sreenivasulu, G., Rasheeda, M. K., & Senthilkumaran, B. (2006). Thiourea-induced thyroid hormone depletion impairs testicular recrudescence in the air-breathing catfish, Clarias gariepinus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 144(1), 1-10. DOI: https://doi.org/10.1016/j.cbpa.2006.01.017
- 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. DOI: https://doi.org/10.1016/j.ygcen.2018.04.023
- Yamamura, T., Yasuo, S., Hirunagi, K., Ebihara, S., & Yoshimura, T. (2006). T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res., 324, 175–179. DOI: https://doi.org/10.1007/s00441-005-0126-8
- Yoshiura, Y., Sohn, Y. C., Munakata, A., Kobayashi, M., & Aida, K. (1999). Molecular cloning of the cDNA encoding the β subunit of thyrotropin and regulation of its gene expression by thyroid hormones in the goldfish, Carassius auratus. Fish Physiology and Biochemistry, 21(3), 201-210. DOI: https://doi.org/10.1023/A:1007884527397
References
Allan, E. R., & Habibi, H. R. (2012). Direct effects of triiodothyronine on production of anterior pituitary hormones and gonadal steroids in goldfish. Molecular Reproduction and Development, 79(9), 592-602. DOI: https://doi.org/10.1002/mrd.22066
Biswas, A. K., Seoka, M., Tanaka, Y., Takii, K., & Kumai, H. (2006). Effect of photoperiod manipulation on the growth performance and stress response of juvenile red sea bream (Pagrus major). Aquaculture, 258(1-4), 350-356. DOI: https://doi.org/10.1016/j.aquaculture.2006.03.048
Coimbra, A. M., Reis-Henriques, M. A., & Darras, V. M. (2005). Circulating thyroid hormone levels and iodothyronine deiodinase activities in Nile tilapia (Oreochromis niloticus) following dietary exposure to Endosulfan and Aroclor 1254. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 141(1), 8-14. DOI: https://doi.org/10.1016/j.cca.2005.04.006
Cyr, D. G., & Eales, J. G. (1996). Interrelationships between thyroidal and reproductive endocrine systems in fish. Reviews in Fish Biology and Fisheries, 6(2), 165-200. DOI: https://doi.org/10.1007/BF00182342
Flood, D. E., Fernandino, J. I., & Langlois, V. S. (2013). Thyroid hormones in male reproductive development: evidence for direct crosstalk between the androgen and thyroid hormone axes. General and comparative endocrinology, 192, 2-14. DOI: https://doi.org/10.1016/j.ygcen.2013.02.038
Furlow, J. D., & Neff, E. S. (2006). A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends in Endocrinology & Metabolism, 17(2), 40-47. DOI: https://doi.org/10.1016/j.tem.2006.01.007
Gereben, B., Zavacki, A. M., Ribich, S., Kim, B. W., Huang, S. A., Simonides, W. S., .Bianco, A. C. (2008). Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocrine reviews, 29(7), 898-938. DOI: https://doi.org/10.1210/er.2008-0019
Hernandez, A., Quignodon, L., Martinez, M. E., Flamant, F., & St. Germain, D. L. (2010). Type 3 deiodinase deficiency causes spatial and temporal alterations in brain T3 signaling that are dissociated from serum thyroid hormone levels. Endocrinology, 151(11), 5550-5558. DOI: https://doi.org/10.1210/en.2010-0450
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. DOI: https://doi.org/10.1016/j.ygcen.2019.113264
Hurlburt, M. E. (1977). Role of the thyroid gland in ovarian maturation of the goldfish, Carassius auratus L. Canadian journal of zoology, 55(11), 1906-1913. DOI: https://doi.org/10.1139/z77-244
Kumari, P., Kumar, M., Sehgal, N., & Aggarwal, N. (2020). In silico analysis of kiss2, expression studies and protein–protein interaction with gonadotropin-releasing hormone 2 (GnRH2) and luteinizing hormone beta (LHβ) in Heteropneustes fossilis. Journal of Biomolecular Structure and Dynamics, 1-15. DOI: https://doi.org/10.1080/07391102.2020.1860820
Larsen, D. A., Dickey, J. T., & Dickhoff, W. W. (1997). Quantification of salmon α-and thyrotropin (TSH) β-subunit messenger RNA by an RNase protection assay: Regulation by thyroid hormones. General and Comparative Endocrinology, 107(1), 98-108. DOI: https://doi.org/10.1006/gcen.1997.6900
Leatherland, J. F., Lin, L., Down, N. E., & Donaldson, E. M. (1989). Thyroid hormone content of eggs and early developmental stages of five Oncorhynchus species. Canadian Journal of Fisheries and Aquatic Sciences, 46(12), 2140-2145. DOI: https://doi.org/10.1139/f89-264
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. DOI: https://doi.org/10.3389/fendo.2020.00175
Morais, R. D. V. S., Nóbrega, R. H., Gómez-González, N. E., Schmidt, R., Bogerd, J., França, L. R., & Schulz, R. W. (2013). Thyroid hormone stimulates the proliferation of Sertoli cells and single type A spermatogonia in adult zebrafish (Danio rerio) testis. Endocrinology, 154(11), 4365-4376. DOI: https://doi.org/10.1210/en.2013-1308
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. DOI: https://doi.org/10.1016/j.mce.2016.08.045
Norberg, B., Brown, C. L., Halldorsson, O., Stensland, K., & Björnsson, B. T. (2004). Photoperiod regulates the timing of sexual maturation, spawning, sex steroid and thyroid hormone profiles in the Atlantic cod (Gadus morhua). Aquaculture, 229(1-4), 451-467. DOI: https://doi.org/10.1016/S0044-8486(03)00393-4
Pant, D. R., Ila, K., Sahu, U.B., & Sehgal, N. (2023). 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). Journal of Applied and Natural Science, 15(1).
Power, D. M., Llewellyn, L., Faustino, M., Nowell, M. A., Björnsson, B. T., Einarsdóttir, I. E., & Sweeney, G. E. (2001). Thyroid hormones in growth and development of fish. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 130(4), 447-459. DOI: https://doi.org/10.1016/S1532-0456(01)00271-X
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. DOI: https://doi.org/10.1007/s11010-020-03873-w
Sehgal, A., & Sundararaj, B. I. (1970). Effects of various photoperiodic regimens on the ovary of the catfish, Heteropneustes fossilis (Bloch) during the spawning and the postspawning periods. Biology of Reproduction, 2(3), 425-434. DOI: https://doi.org/10.1095/biolreprod2.3.425
Sohn, Y. C., Yoshiura, Y., Kobayashi, M., & Aida, K. (1999). Seasonal changes in mRNA levels of gonadotropin and thyrotropin subunits in the goldfish, Carassius auratus. General and comparative endocrinology, 113(3), 436-444. DOI: https://doi.org/10.1006/gcen.1998.7224
Swapna, I., Rajasekhar, M., Supriya, A., Raghuveer, K., Sreenivasulu, G., Rasheeda, M. K., & Senthilkumaran, B. (2006). Thiourea-induced thyroid hormone depletion impairs testicular recrudescence in the air-breathing catfish, Clarias gariepinus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 144(1), 1-10. DOI: https://doi.org/10.1016/j.cbpa.2006.01.017
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. DOI: https://doi.org/10.1016/j.ygcen.2018.04.023
Yamamura, T., Yasuo, S., Hirunagi, K., Ebihara, S., & Yoshimura, T. (2006). T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res., 324, 175–179. DOI: https://doi.org/10.1007/s00441-005-0126-8
Yoshiura, Y., Sohn, Y. C., Munakata, A., Kobayashi, M., & Aida, K. (1999). Molecular cloning of the cDNA encoding the β subunit of thyrotropin and regulation of its gene expression by thyroid hormones in the goldfish, Carassius auratus. Fish Physiology and Biochemistry, 21(3), 201-210. DOI: https://doi.org/10.1023/A:1007884527397