MELATONIN PROTECTS AGAINST OXIDATIVE DAMAGE IN SPLEEN AND DETERIORATION OF IMMUNE FUNCTION IN FORCED SWIM-STRESSED LABORATORY MICE

Abstract views: 28 / PDF downloads: 71

Authors

Keywords:

Forced swimming stress, melatonin, spleen, oxidative stress, MT1 & MT2 receptors

Abstract

Stress is an external or internal stimulus that interferes with the normal physiology and homeostatic status of an individual. Acute stress is the short-term exposure to stress and chronic stress involves prolonged exposure to stress. Forced swimming stress is a widely accepted model to study physiological stress in laboratory animals. Melatonin is a powerful antioxidant and modulator of the immune system. Melatonin modulates physiological activities through its high-affinity MT1 and MT2 receptors and directly through scavenging free radicals. The present study evaluated the involvement of melatonin in the attenuation of forced swimming stressed induced oxidative stress, splenocyte proliferation, intracellular ROS generation, and phagocytic index of macrophages. Acute and chronic swimming stress caused an increase in lipid peroxidation and reduced the antioxidant enzyme (SOD and catalase) activity in the spleen of mice. Melatonin supplementation to both chronic and acute stressed groups decreased lipid peroxidation and enhanced the antioxidant activity (SOD and catalase) in the spleen of mice.  Melatonin attenuated the suppression of phagocytic activity, and splenocyte proliferation caused by both acute and chronic swim stress. Swim stress caused increased MT1 and MT2 receptor expression in the spleen of mice. Increased expression of melatonin receptors might be responsible for melatonin-mediated induction of antioxidant enzyme activity during stressed conditions in mice. Therefore, the present study may suggest that melatonin attenuates the swim-stressed induced oxidative stress, and suppression of immune functions through modulation of MT1 and MT2 receptors.

References

Porsolt, R.D., Lepichon, M., Jalfre, M. (1977): Depression: A new animal model sensitive to antidepressant treatments. Nature 266:730-732. https://doi.org/10.1038/266730a0.

Marklund, S., Marklund, G. (1974): Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry 47: 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x.

Kramer, K., Dijkstra, H., Bast, A. (1993): Control of physical exercise of rats in a swimming basin. Physiology and Behaviour 53:271-276. https://doi.org/10.1016/0031-9384(93)90204-s.

Nagaraja, H.S., Jeganathan, P.S. (1999): Forced swimming stress induced changes in the physiological and biochemical parameters in albino rats. Indian Journal of Physiology and Pharmacology 43:53-59

Greenen, D., Buttrick, P., Scheuer, J. (1988): Cardiovascular and hormonal responses to swimming and running in the rat. Journal of Applied Physiology 65:116-123. https://doi.org/10.1152/jappl.1988.65.1.116.

Tan, N., Morimoto, K., Sugiura, T., Morimoto, A., Murakami, N. (1992): Effects of running training on the blood glucose and lactate in rats during rest and swimming. Physiology and Behaviour 51:927–931. https://doi.org/10.1016/0031-9384(92)90072-a.

Blecha, F. (2000): Immune system response to stress. In The biology of animal stress: basic principles and implications for animal welfare 111-121. Wallingford UK: CABI Publishing.

Dhabhar, F. (1998): Stress-Induced Enhancement of Cell-Mediated Immunity. Annals of the New York Academy of Sciences 840:359–372. https://doi.org/10.1111/j.1749-6632.1998.tb09575.x.

Glaser, R., Kiecolt-Glaser, J.K. (2005): Stress-induced immune dysfunction: Implications for health. Nature Reviews Immunology 5:243–251. https://doi.org/10.1038/nri1571.

Pavlou, S., Wang, I., Xu, H., Chen, M. (2017): Higher phagocytic activity of thioglycollate-elicited peritoneal macrophages is related to metabolic status of the cells. Journal of Inflammation 14:4. https://doi.org/10.1186/s12950-017-0151-x.

Zhang, X., Goncalves, R., Mosser, D.M. (2008): The isolation and characterization of murine macrophages. Current Protocols in Immunology 83:14. https://doi.org/10.1002/0471142735.im1401s83.

Hwang, H.J., Kwak, Y.S., Yoon, G.A., Kang, M.H., Park, J.H., Le, B.K., Kim, S.J., Um, S.Y., Kim, Y.M. (2007): Combined effects of swim training and ginseng supplementation on exercise performance time, ROS, lymphocyte proliferation, and DNA damage following exhaustive exercise stress. International Journal for Vitamin and Nutrition Research 77(4): 289-296. https://doi.org/10.1024/0300-9831.77.4.289.

Liu, J., Mori, A. (1999): Stress, aging, and oxidative damage. Neurochemical Research 24:1479-1497. https://doi.org/10.1023/a:1022597010078.

Betteridge, D.J. (2000): What is Oxidative Stress?. Metabolism 49:3-8. https://doi.org/10.1016/S0026-0495(00)80077-3.

Wang, F., Zhang, Y.Q. (2015): Bioconjugation of Silk Fibroin Nanoparticles with enzyme and peptide and their characterization. Advances in Protein Chemistry and Structural Biology 98:263-291. https://doi.org/10.1016/bs.apcsb.2014.11.005.

Liu, X., Kokare, C. (2023): Microbial enzymes of use in industry. InBiotechnology of microbial enzymes. 405-444. Academic Press.

Xia, M.Z., Liang, Y.L., Wang, H., Chen, X., Huang, Y.Y., Zhang, Z.H., Chen, Y.H., Zhang, C., Zhao, M., Xu, D.X., Song, L.H. (2012): Melatonin modulates TLR4-mediated inflammatory genes through MyD88- and TRIF-dependent signaling pathways in lipopolysaccharide-stimulated RAW264.7 cells. Journal of Pineal Research 53:325–334. https://doi.org/10.1111/j.1600-079X.2012.01002.x.

Jockers, R., Delagrange, P., Dubocovich, M.L., Markus, R.P., Renault, N., Tosini, G., Cecon, E., Zlotos, D.P. (2016): Update on melatonin receptors. British Journal of Pharmacology 173:2702–2725. https://doi.org/10.1111/bph.13536.

Sharafati-Chaleshtori, R., Shirzad, H., Rafieian-Kopaei, M., Soltani, A. (2017): Melatonin and human mitochondrial diseases. Journal of Research in Medical Sciences 22:2. https://doi.org/10.4103/1735-1995.199092.

Pang, C.S., Pang, S.F. (1992): High affinity specific binding of 2-[125I] iodomelatonin by spleen membrane preparations of chicken. Journal of Pineal Research 12:167–173. https://doi.org/10.1111/j.1600-079x.1992.tb00044.x.

Calvo, J.R., Rafil-El-Idrissi, M., Pozo, D., Guerrero, J.M. (1995): Immunomodulatory role of melatonin: Specific binding sites in human and rodent lymphoid cells. Journal of Pineal Research 18:119–126. https://doi.org/10.1111/j.1600-079x.1995.tb00149.x.

Ahmad, R., Haldar, C. (2010): Photoperiodic regulation of MT1 and MT2 melatonin receptor expression in spleen and thymus of a tropical rodent Funambulus pennanti during reproductively active and inactive phases. Chronobiology International 27(3): 446-462. https://doi.org/10.3109/07420521003666408.

Acharjee, S., Singh, S.S. (2015): Melatonin and thermal stress regulate differential expression of heat shock proteins and melatonin receptors in spleen of mice. Indian Journal of Pharmaceutical and Biological Research 3:36-47. https://doi.org/10.30750/ijpbr.3.1.7.

Ohkawa, H., Ohishi, N., Yagi, K. (1979): Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry. 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3.

Das, K., Samanta, L., Chainy, G.B.N. (2000): A modified spectrophotometric assay of superoxide dismutase using nitrate formation by superoxide radicals. Indian Journal of Biochemistry and Biophysics 37:201–204.

Sinha, A.K. (1972): Colorimetric assay of catalase. Analytical Biochemistry 47:389-394.

Hadwan, M.H. (2016): New method for assessment of serum catalase activity. Indian Journal of Science Technology 9:1-5. https://doi.org/10.17485/ijst/2016/v9i4/80499.

Majewski, P., Dziwinski, T., Pawlak, J., Waloch, M., Skwarlo-Sonta, K. (2005): Anti-inflammatory and opioid-mediated effects of melatonin on experimental peritonitis in chicken. Life Science 76:1907-1920. https://doi.org/10.1016/j.lfs.2004.04.062.

Roy, B., Rai, U. (2008): Role of adrenoceptor-coupled second messenger system in sympatho-adrenomedullary modulation of splenic macrophage functions in live fish, Channa punctatus. General and Comparative Endocrinology 155:298-306. https://doi.org/10.1016/j.ygcen.2007.05.008.

Singh, S.S., Laskar, P., Acharjee, S. (2015): Age- and sex- dependent effect of exogenous melatonin on expression pattern of melatonin receptor (MT1 and MT2) proteins in spleen of mice. Biological Rhythm Research 46:403–415. https://doi.org/10.1080/09291016.2015.1020198.

Connor, T.J., Kelly, J.P., Leonard, B.E. (1997): Forced Swim Test-Induced Neurochemical, Endocrine, and Immune Changes in the Rat. Pharmacology Biochemistry and Behaviour 58:961-967. https://doi.org/10.1016/s0091-3057(97)00028-2.

Kurutas, E.B. (2016): The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutrition Journal 15(1):71. https://doi.org/10.1186/s12937-016-0186-5.

Signorini, C., Felice, C.D., Durand, T., Oger, C., Galano, J.M., Leoncini, S., Pecorelli, A., Valacchi, G., Ciccoli, L., Hayek, J. (2013): Isoprostanes and 4-Hydroxy-2-nonenal: Markers or Mediators of Disease? Focus on Rett Syndrome as a Model of Autism Spectrum Disorder. Oxidative Medicine and Cellular Longevity 1-10. https://doi.org/10.1155/2013/343824.

Nayanatara, A.K., Nagaraja, H.S., Anupama, B.K. (2005): The effect of repeated swimming stress on organ weights and lipid peroxidation in rats. The Thai Journal of Physiological Sciences 18:3-9.

Claustrat, B., Brun, J., Chazot, G. (2005): The basic physiology and pathophysiology of melatonin. Sleep Medicine Review 9:11–24. https://doi.org/10.1016/j.smrv.2004.08.001.

Duan, F.F., Guo, Y., Li, J.W., Yuan, K. (2017): Antifatigue Effect of Luteolin-6-C-Neohesperidoside on Oxidative Stress Injury Induced by Forced Swimming of Rats through Modulation of Nrf2/ARE Signaling Pathways. Oxidative Medicine Cellular Longevity 2017:1-13. https://doi.org/10.1155/2017/3159358.

Borah, M., Sarma, P., Das, S. (2014): A Study of the Protective Effect of Triticum aestivum L. in an Experimental Animal Model of Chronic Fatigue Syndrome. Pharmacognosy Research 6:285-291. https://doi.org/10.4103/0974-8490.138251.

Sutradhar, S., Deb, A., Singh, S.S. (2020): Melatonin attenuates diabetes-induced oxidative stress in spleen and suppression of splenocyte proliferation in laboratory mice. Archives of Physiology and Biochemistry 128(5):1401-12. https://doi.org/10.1016/0003-2697(72)90132-7.

Sutradhar, S., Deb, A., Singh, S.S. (2022): Protective efficacy of melatonin and insulin against LPS caused toxicity in diabetic mice. Immunopharmacology and Immunotoxicology 44(6): 902-14. http://dx.doi.org/10.1080/08923973.2022.2093739.

Singh, S.S., Deb, A., Sutradhar, S. (2019): Effect of melatonin on arsenic-induced oxidative stress and expression of MT1 and MT2 receptors in the kidney of laboratory mice. Biological Rhythm Research 51:1216-1230. https://doi.org/10.1080/09291016.2019.1566993.

Downloads

Published

2024-02-06

How to Cite

Shiv Shankar Singh, Subhrata Sarma, Kashyap, A., & Chakrabarti, A. (2024). MELATONIN PROTECTS AGAINST OXIDATIVE DAMAGE IN SPLEEN AND DETERIORATION OF IMMUNE FUNCTION IN FORCED SWIM-STRESSED LABORATORY MICE. Journal of Applied Biological Sciences, 18(1), 78–93. Retrieved from https://jabsonline.org/index.php/jabs/article/view/1271

Issue

Section

Articles