Oxidative Damage and Apoptosis Induction by L-thyroxine in the Spleen of a Tropical Bird Perdicula asiatica: Rescue by Melatonin

Authors

  • Pineal Research Laboratory, Department of Zoology, Banaras Hindu University, Varanasi - 221005
  • Pineal Research Laboratory, Department of Zoology, Banaras Hindu University, Varanasi - 221005
  • Pineal Research Laboratory, Department of Zoology, Banaras Hindu University, Varanasi - 221005

DOI:

https://doi.org/10.18311/jer/2019/26152

Keywords:

Anti-KLH IgG, Apoptosis, L-Thyroxin, Melatonin, Oxidative Stress

Abstract

Avian thyroid gland is known to influence the immunity and reproduction in an opposite manner. In this study, we evaluated the immunostimulatory, anti-oxidative and anti-apoptotic roles of melatonin in a tropical bird, Indian jungle bush quail, Perdicula asiatica, having L-thyroxine (thyrotoxicity)-induced oxidative stress. Administration of L-thyroxine (100 μg/kg body weight) enhanced the thyroidal lipid peroxidase (LPO), with a parallel decrease in the levels of antioxidant enzyme (SOD, GPx, CAT, MDA & NO) activities. Cellular immune response (%SR) and humoral immune response (anti-KLH-IgG level) of splenocytes along with general hematological parameters (TLC, LC & HF/L ratio) decreased significantly upon L-thyroxine treatment. Further, decrease in circulatory anti-inflammatory cytokines IL-2 and TNFα suggested drastic effects of induced thyrotoxicity (elevated levels of T3 & T4) on immunity. Melatonin pre-treatment (25 μg/100g BW) during evening hours (prior to L-thyroxine treatment in the afternoon) for 30 days circumvented the deleterious effects of L-thyroxine-induced oxidative stress (level of Corticosterone) and apoptosis index of the avian spleen. Our results clearly indicate the potential of melatonin in rescuing/reducing the thyrotoxicity-induced oxidative damage to avian immunity.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Hassman R, Weetman AP, Gunn C, Stringer BMJ. Wynford Thomas D, Hall R, McGregor, AM. The effects of hypothyroidism on autoimmune thyroiditis in rat. Endocrinology. 1985; 166:12-53.

Haldar C, Singh R. Pineal modulation of thymus and immune function in a seasonally breeding rodent, F. pennanti. J Exp Zool. 2001; 286:90-98. https://doi.org/10.1002/1097-010X(20010201)289:2<90::AIDJEZ2> 3.0.CO;2-S.

Rao G, Verma R, Mukherjee A, Haldar C, Agrawal NK. Melatonin alleviates hyperthyroidism induced oxidative stress and neuronal cell death in hippocampus of aged female golden hamster, Mesocricetus auratus. Exp Gerontol. 2016; 82:125-130. https://doi.org/10.1016/j.exger.2016.06.014. PMid:27374868.

Poppe K, Velkeniers B, Glinoer D. Thyroid disease and female reproduction. Clin Endocrinol. 2007; 66(3):309321. https://doi.org/10.1111/j.1365-2265.2007.02752.x. PMid:17302862.

Singh SS, Haldar C. Melatonin prevents testosteroneinduced suppression of immune parameters and splenocyte proliferation in Indian tropical jungle bush quail, Perdicula asiatica. Gen Comp Endocrinol. 2005; 141:226-232. https:// doi.org/10.1016/j.ygcen.2005.01.005. PMid:15804509.

Singh SS, Haldar C. Peripheral melatonin modulates seasonal immunity and reproduction of Indian tropical male bird, Perdicula asiatica. Comp Biochem Physiol A. 2007; 146:446-450. https://doi.org/10.1016/j.cbpa.2006.12.024. PMid:17257874.

Singh SS, Haldar C, Rai S. Melatonin and differential effect of L-thyroxine on immune system of Indian tropical bird, Perdicula asiatica. Gen Comp Endocrinol. 2006; 145:215-21. https://doi.org/10.1016/j.ygcen.2005.09.007. PMid:16243326.

Haldar C, Ghosh M. Annual pineal and testicular cycle in the Indian jungle bush quail, Perdicula asiatica, with reference to the effect of pinealectomy. Gen Comp Endocrinol. 1990; 77(1):150-57. https://doi.org/10.1016/00166480(90)90216-9.

Wiktorska JA, Lewinski A, Sewerynek E. Effects of different antioxidants on lipid peroxidation in brain homogenates, induced by L-thyroxine administration in rats. NeuroEndocrinol Lett. 2005; 26(6):704-708.

Ots I, Murumí„gii A, Híµrak P. Haematological health state indices of reproducing Great Tits: Methodology and sources of natural variation. Funct Ecol. 1998; 12(4):700707. https://doi.org/10.1046/j.1365-2435.1998.00219.x.

Ohkawa H, Ohishi N, Yagi K. Reaction of linoleic acid hydroperoxide with thiobarbituric acid. J Lip Res.

; 19:1053-1057. https://doi.org/10.1016/S00222275(20)40690-X.

Kumar J, Haldar C, Verma R. Fluoride Compromises Testicular Redox Sensor, Gap Junction Protein, and Metabolic Status: Amelioration by Melatonin. Biol Trace Elem Res. 2020; 196(2):552-564. https://doi.org/10.1007/ s12011-019-01946-6. PMid:31828722.

Kumar J, Haldar C, Verma R. (2020). Effect of quinalphos on testes of long day seasonal breeder golden hamster, Mesocricetus auratus. J Sc Res. 64(1):97-102. https://doi.org/10.37398/JSR.2020.640114.

Kumar J, Verma R, Haldar C. (2021). Melatonin ameliorates Bisphenol S induced testicular damages by modulating Nrf-2/HO-1 and SIRT-1/FOXO-1 expressions. Environ Toxicol 36(3):396-407. https://doi.org/10.1002/tox.23045. PMid:33098627.

Das K, Samanta L, Chainy GBN. A modified spectrophotometric assay of superoxide dismutase using nitrite formation by superoxide radicals. Ind J Biochem Biophys. 2000; 37:201-204.

Aebi H. 1974. Catalase. In: Bergmeyer, H.U. (Ed.) Methods of Enzymatic Analysis. Academic Press, New York; p. 673684. https://doi.org/10.1016/B978-0-12-091302-2.50032-3.

Sastry KVH, Moudgal RP, Mohan J, Tyagi, JS, Rao GS. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal Biochem. 2002; 306:79-82. https://doi.org/10.1006/abio.2002.5676. PMid:12069417.

Mantha SV, Prasad M, Kalr, J, Prasad K. Antioxidant enzymes in hypercholesterolemia and effect of vitamin E in rabbits. Atherosclerosis. 1993; 101:1351-44. https://doi.org/10.1016/0021-9150(93)90110-G.

Demas, GE, Chefer, V, Talan, MI, Nelson, RJ. Metabolic costs of mounting an antigen stimulated immune response in adult and aged C57BL/6J mice. Am J Physiol. 1997; 273:1631-1637. https://doi.org/10.1152/ ajpregu.1997.273.5.R1631. PMid: 9374803.

Ahmad R, Haldar C. Immune responses to lipopolysaccharide challenge in a tropical rodent, Funambulus pennanti: photoperiod entrainment and sex differences. Stress. 2012; 15(2):172-183. https://doi.org/10 .3109/10253890.2011.606515. PMid:21854165.

Goswami S, Haldar C. UVB irradiation severely induces systemic tissue injury by augmenting oxidative load in a tropical rodent: Efficacy of melatonin as an antioxidant. J Photochem Photobiol B. 2014; 141:84-92. https://doi.org/10.1016/j.jphotobiol.2014.08.027. PMid:25463654.

Monteverdi GH, Di Giulio RT. Vitellogenin association and oocytic accumulation of thyroxine and 3, 5, 3'-triiodothyronine in gravid Fundulus heteroclitus. Gen Comp Endocrinol. 2000; 120:198-211. https://doi.org/10.1006/gcen.2000.7551. PMid:11078631.

Volkoff H, Wourms JP, Amesbury E, Snelson FF. Structure of the thyroid gland, serum thyroid hormones, and the reproductive cycle of the Atlantic stingray, Dasyatis sabina. J Exp Zool. 1999; 284:505-516. https://doi.org/10.1002/(SICI)1097-010X(19991001)284:5<505::AIDJEZ6> 3.0.CO;2-1.

Matty AJ. Fish Endocrinology. CROOM HELM. 1985.

Dardente H, Hazlerigg DG, Ebling FJP. Thyroid hormone and seasonal rhythmicity. Fron Endocrinol. 2014; 5:1-11. https://doi.org/10.3389/fendo.2014.00019. PMid:24616714 PMCid:PMC3935485.

Sahoo DK, Roya A, Chainy GBN. Protective effects of vitamin E and curcumin on l-thyroxine-induced rat testicular oxidative stress. Chem-Biol Interact. 2008; 176:121-128. https://doi.org/10.1016/j.cbi.2008.07.009. PMid:18723006.

Jena S, Chainy GBN. Regulation of expression of antioxidant enzymes by vitamin E and curcumin in L-thyroxineinduced oxidative stress in rat renal cortex. Mol Biol Reports. 2011; 38(2):1047-1054. https://doi.org/10.1007/ s11033-010-0201-4. PMid:20574713

Downloads

Published

2021-03-31

How to Cite

Kumar Verma, V., Haldar, C., & Pal, S. (2021). Oxidative Damage and Apoptosis Induction by L-thyroxine in the Spleen of a Tropical Bird <i>Perdicula asiatica</i>: Rescue by Melatonin. Journal of Endocrinology and Reproduction, 23(2), 109–122. https://doi.org/10.18311/jer/2019/26152

Issue

Section

Original Research

Most read articles by the same author(s)

1 2 3 > >>