Effects of L-Thyroxine on the Reproductive Functions of the Indian Pygmy Field Mouse Mus terricolor
Keywords:Mus terricolor, Seasonal reproduction, Thyroid, Reproduction, Tropical rodent
Besides being potent regulators of energy balance, thyroid hormones are necessary for the maintenance of seasonal reproductive changes in many species of mammals and birds. The thyroid gland is known to be crucial for the seasonal transition in seasonal breeders from breeding to non-breeding. Many workers have reported that thyroid ablation prevents the animal from entering the non-breeding state in both males and females of different species of animals and, in such a situation, the breeding state is sustained indefinitely. No report exists to date about the involvement of the thyroid gland in the reproduction of the pygmy field mouse Mus terricolor. L-thyroxine was administered subcutaneously to both male and female mice for 15 consecutive days during the reproductively active phase. L-thyroxine treatment led to a significant reduction in the weights of gonads and accessory sex organs along with biochemical constituents like epididymal sialic acid, seminal vesicular fructose and uterine protein. Regressive changes in the histology of the gonads and accessory sex organs were observed which can be attributed to the reduced levels of plasma testosterone in males and plasma estradiol and progesterone in females of the L-thyroxine-treated mice. However, there was a significant increase in the levels of plasma T3, T4, and gonadal cholesterol in both sexes following L-thyroxine treatment. Both hypo- and hyper-thyroidism can influence gonadal activity. The observations in the present study suggest that hyperthyroidism leads to the transition of reproductively active gonads to inactivity substantiating the hypothesis that high levels of thyroxine can accelerate the reproductive inactivity in this rodent.
Stetson MH, Tate-Ostroff B. Hormonal regulation of the annual reproductive cycle of golden hamsters. General and Comparative Endocrinology. 1981; 45(3):329-44. https://doi.org/10.1016/0016-6480(81)90073-3 PMID:6795080
Woitkewitsch AA. Dependence of seasonal periodicity in gonadal changes on the thyroid gland in Sturnus vulgaris L. In: CR (Doklady) Acad Sci URSS. 1940. p. 741-5.
Vriend J. Effects of melatonin and thyroxine replacement on thyrotropin, luteinizing hormone, and prolactin in male hypothyroid hamsters. Endocrinology. 1985; 117(6):2402-7. https://doi.org/10.1210/endo-117-6-2402 PMID:3933963
Verma R, Haldar C. Photoperiodic modulation of thyroid hormone receptor (TR-α), deiodinase-2 (Dio-2) and glucose trans¬porters (GLUT 1 and GLUT 4) expression in testis of adult golden hamster, Mesocricetus auratus. Journal of Photochemistry and Photobiology B: Biology. 2016; 165:351-8. https://doi.org/10.1016/j.jphotobiol.2016.10.036 PMID:27838488
Haldar C, Srivastava M. Pineal gland and annual thyroid function of a tropical mammal Funambulus pennanti. Proceedings of National Academy of Science India. 1988; 58:49-54.
Haldar C, Shavali SS, Singh S. Photoperiodic response of pineal-thyroid axis of the female Indian palm squirrel, Funambulus pennanti. Journal of Neural Transmission/General Section JNT. 1992; 90(1):45-52. https://doi.org/10.1007/BF01250517 PMID:1466877
Anderson GM, Hardy SL, Valent M, et al. Evidence that thyroid hormones act in the ventromedial preoptic area and the premam¬millary region of the brain to allow the termination of the breeding season in the ewe. Endocrinology. 2003; 144(7):2892-901. https://doi.org/10.1210/en.2003-0322 PMID:12810544
Jallageas M, Assenmacher I. Effects of castration and thyroidectomy on the annual biological cycles of the edible dormouse Glis glis. General and Comparative Endocrinology. 1986; 63(2):301-8. https://doi.org/10.1016/0016-6480(86)90168-1 PMID:3781234
Haldar C, Ghosh M. Effect of pinealectomy and different 5-methoxyindole on thyroid gland function of the Indian jungle bush quail, Perdicula asiatica. New Delhi: Hindustan Publishing Corporation (India); 1996.
Bar MS. Role of thyroxine and prolactin in the testicular status of spotted munia (Lonchura punctulata). Journal of Environmental Biology. 2006; 27(1):141.
Inuwa I, Williams MA. Morphometric study on the uterine horn and thyroid gland in hypothyroid, and thyroxine treated hypothyroid rats. Journal of Anatomy. 1996; 188(Pt 2):383.
Hatsuta M, Abe K, Tamura K, et al. Effects of hypothyroidism on the estrous cycle and reproductive hormones in mature female rat. European Journal of Pharmacology. 2004; 486(3):343-8. https://doi.org/10.1016/j.ejphar.2003.12.035 PMID:14985057
Jenny V, Bertalanffy FD, Ralecewicz TA. The effects of melatonin and hypothyroidism on estradiol and gonadotropin levels in female Syrian Hamsters. Biology of Reproduction. 1987; 36:719-728. https://doi.org/10.1095/biolreprod36.3.719 PMID:3109508
Cecconi S, Rucci N, Scaldaferri ML, Thyroid hormone effects on mouse oocyte maturation and granulosa cell aromatase activity. Endocrinology. 1999; 140(4):1783-8. https://doi.org/10.1210/endo.140.4.6635 PMID:10098516
Schwartz MW, Figlewicz DP, Baskin DG, et al. Insulin in the brain: A hormonal regulator of energy balance. Endocrine Reviews. 1992; 13(3):387-414. https://doi.org/10.1210/edrv-13-3-387 PMID:1425482
Boswell T, Woods SC, Kenagy GJ. Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. General and Comparative Endocrinology. 1994; 96(3):339-46. https://doi.org/10.1006/gcen.1994.1189 PMID:7883140
Capen CC, Martin SL. The thyroid gland. Veterinary Endocrinology and Reproduction. McDonald LE, Pineda MH, editors 4th ed. Philadelphia, PA: Lea and Febiger. 1989; p. 58-91.
Arora S, Basu P, Singh P, Haldar C. Reproductive seasonality in the Indian pygmy field mouse, Mus terricolor. Biological Rhythm Research. 2015; 46(1):13-32. https://doi.org/10.1080/09291016.2014.939443
Basu P, Singaravel M, Haldar C. L-5-hydroxytryptophan resets the circadian locomotor activity rhythm of the nocturnal Indian pygmy field mouse, Mus terricolor. Naturwissenschaften. 2012; 99(3):233-9. https://doi.org/10.1007/s00114-012-0893-5 PMID:22331255
Basu P, Singaravel M. Accurate and precise circadian locomotor activity rhythms in male and female Indian pygmy field mice, Mus terricolor. Biological Rhythm Research. 2013; 44(4):531-9. https://doi.org/10.1080/09291016.2012.721587
Rai S, Haldar C, Singh SS. Trade-off between L-thyroxin and melatonin in immune regulation of the Indian palm squirrel, Funambulus pennanti during the reproductively inactive phase. Neuroendocrinology. 2005; 82(2):103-10. https://doi. org/10.1159/000091034 PMID:16424677
Aminoff D. Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids. Biochemical Journal. 1961; 81(2):384. https://doi.org/10.1042/bj0810384 PMID:13860975 PMCID:PMC1243351
Lindner HR, Mann T. Relationship between the content of androgenic steroids in the testes and the secretory activity of the seminal vesicles in the bull. Journal of Endocrinology. 1960; 21(3):341-NP. https://doi.org/10.1677/joe.0.0210341 PMID:13762385
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein- dye binding. Analytical Biochemistry. 1976; 72(1-2):248-54. https://doi.org/10.1016/0003-2697(76)90527-3 PMID:942051
Schultze AB, Noonan J. Thyroxine administration and reproduction in rats. Journal of Animal Science. 1970; 30(5):774-6. https:// doi.org/10.2527/jas1970.305774x PMID:5420311
O’Callaghan D, Wendling A, Karsch FJ, Roche JF. Effect of exogenous thyroxine on timing of seasonal reproductive transitions in ewes. Biology of Reproduction. 1993; 49(2):311-5. https://doi.org/10.1095/biolreprod49.2.311 PMID:8373954
Webster JR, Moenter SM, Woodfill CJ, Karsch FJ. Role of the thyroid gland in seasonal reproduction. II. Thyroxine allows a season-specific suppression of gonadotropin secretion in sheep. Endocrinology. 1991; 129(1):176-83. https://doi.org/10.1210/ endo-129-1-176 PMID:2055181
Thrun LA, Dahl GE, Evans NP, Karsch FJ. A critical period for thyroid hormone action on seasonal changes in reproductive neuroendocrine function in the ewe. Endocrinology. 1997; 138(8):3402-9. https://doi.org/10.1210/endo.138.8.5341 PMID:9231794
Shi ZD, Barrell GK. Requirement of thyroid function for the expression of seasonal reproductive and related changes in red deer (Cervus elaphus) stags. Reproduction. 1992; 94(1):251-9. https://doi.org/10.1530/jrf.0.0940251 PMID:1552486
Viguie C, Battaglia DF, Krasa HB, et al. Thyroid hormones act primarily within the brain to promote the seasonal inhibition of luteinizing hormone secretion in the ewe. Endocrinology. 1999; 140(3):1111-7. https://doi.org/10.1210/endo.140.3.6543 PMID:10067833
Lechan RM, Fekete C. Role of thyroid hormone deiodination in the hypothalamus. Thyroid. 2005; 15(8):883-97. https://doi. org/10.1089/thy.2005.15.883 PMID:16131331
Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocrine Reviews. 2002; 23(1):38-89. https://doi.org/10.1210/edrv.23.1.0455 PMID:11844744
Barrett P, Ebling FJ, Schuhler S, et al. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology. 2007; 148(8):3608-17. https://doi.org/10.1210/en.2007-0316 PMID:17478556
Watanabe T, Yamamura T, Watanabe M, et al. Hypothalamic expression of thyroid hormone-activating and-inactivating enzyme genes in relation to photorefractoriness in birds and mammals. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 2007; 292(1):R568-72. https://doi.org/10.1152/ajpregu.00521.2006 PMID:17197645
Yasuo S, Yoshimura T, Ebihara S, Korf HW. Photoperiodic Control of TSH--β Expression in the Mammalian Pars Tuberalis has Different Impacts on the Induction and Suppression of the Hypothalamo-Hypopysial Gonadal Axis. Journal of Neuroendocrinology. 2010; 22(1):43-50. https://doi.org/10.1111/j.1365-2826.2009.01936.x PMID:19912473
Hanon EA, Routledge K, Dardente H, et al. Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). Journal of Neuroendocrinology. 2010; 22(1):51-5. https://doi.org/10.1111/j.1365- 2826.2009.01937.x PMID:19912472
Messarah M, Boumendjel A, Chouabia A, et al. Influence of thyroid dysfunction on liver lipid peroxidation and antioxidant status in experimental rats. Experimental and Toxicologic Pathology. 2010; 62(3):301-10. https://doi.org/10.1016/j.etp.2009.04.009 PMID:19540741
Kim SM, Kim SC, Chung IK, et al. Antioxidant and protective effects of Bupleurum falcatum on the L-thyroxine-induced hyperthyroidism in rats. Evidence-based Complementary and Alternative Medicine. 2012; 2012:578497. https://doi. org/10.1155/2012/578497 PMID:22888365 PMCID:PMC3410357