Protective effects of melatonin on mitochondrial injury and neonatal neuron apoptosis induced by maternal hypothyroidism
Impact of melatonin on mitochondrial outer membrane of neonatal brain
Keywords:
Melatonin, mitochondria, propylthiouracyl, hypothyroidism, apoptosis, cytochrome c oxidase, thyroid stimulating hormone, thyroid hormones
Abstract
In the current study, we reported the beneficial effects of melatonin in preventing neonatal neuronal apoptosis induced by maternal hypothyroidism. During the gestation and early lactation stages, the mother rats were given propylthiouracil (PTU) to inhibit their thyroid gland activity which resulted in the increased serum TSH and reduced T4 levels. This maternal hypothyroidism caused neuronal apoptosis of their pups, particularly in the CA3 area of hippocampus. Melatonin administration preserved function of thyroid gland and significantly reduced the apoptosis. Further studies have uncovered the potentially protective mechanisms of melatonin, that is, as a mitochondrial targeted antioxidant, melatonin preserves the mitochondrial outer membrane, inhibits the release of cytochrome C from mitochondria to cytoplasm and down regulates the gene expressions of Bax, along with caspases 3 and 9. Thus, melatonin breaks the mitochondria related apoptotic pathway to suppress the neuronal apoptosis induced by the maternal hypothyroidism. Considering the limited remedies to effectively treat hypothyroidism associated neonatal brain damage, melatonin may provide an alternative method for this disorder.
References
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9. Hidayat M, Haider I, Khurram A, Lone KP (2019) The immunohistochemical localization of Bax in the brain of hypothyroid neonate during maternal melatonin intake. Int. J. Anat. Res. 7 (3): 6901-6905. doi: https://dx.doi.org/10.16965/ijar.2019.259.
10. Xiao Q, Nikodem VM (1998) Apoptosis in the developing cerebellum of the thyroid hormone deficient rat. Front. Bio-science 3 (1): A52-57.
11. Faustino LC, Ortiga-Carvalho TM (2014) Thyroid hormone role on cerebellar development and maintenance: a perspective based on transgenic mouse models. Front. Endocrinol. (Lausanne). 5: 75. doi:10.3389/fendo.2014.00075.
12. Cooke GE, Mullally S, Correia N, O'Mara SM, Gibney J (2014) Hippocampal volume is decreased in adults with hypothyroidism. Thyroid 24 (3): 433-40. doi: 10.1089/thy.2013.0058.
13. Nam SM, Kim JW, Yoo DY et al. (2018) Hypothyroidism increases cyclooxygenase-2 levels and pro-inflammatory response and decreases cell proliferation and neuroblast differentiation in the hippocampus. Mol. Med. Rep. 17 (4): 5782–5788. doi:10.3892/mmr.2018.8605.
14. Becker EB, Bonni A (2004) Cell cycle regulation of neuronal apoptosis in development and disease. Prog. Neurobiol. 72 (1):1-25.
15. Chatonnet F, Picou F, Fauquier T, Flamant F (2011) Thyroid hormone action in cerebellum and cerebral cortex development. J. Thyroid Res. 2011: 145762. doi:10.4061/2011/145762.
16. Osellame LD, Blacker TS, Duchen MR (2012) Cellular and molecular mechanisms of mitochondrial function. Best Pract. Res. Clin. Endocrinol. Metab. 26 (6): 711–723. doi:10.1016/j.beem.2012.05.003.
17. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35 (4): 495–516. doi:10.1080/01926230701320337.
18. Chen X, Guo C, Kong J (2012) Oxidative stress in neurodegenerative diseases. Neural Regen. Res. 7 (5): 376–385. doi:10.3969/j.issn.1673-5374.2012.05.009.
19. Alemu A, Terefe B, Abebe M, Biadgo B (2016) Thyroid hormone dysfunction during pregnancy: A review. Int. J. Reprod. Biomed. (Yazd). 14 (11): 677–686.
20. Miranda A, Sousa N (2018) Maternal hormonal milieu influence on fetal brain development. Brain Behav. 8 (2): e00920. https://doi.org/10.1002/brb3.920.
21. Sahay RK, Nagesh VS (2012) Hypothyroidism in pregnancy. Ind. J. Endocrinol. Metab. 16 (3): 364–370. doi:10.4103/2230-8210.95667.
22. Dirar AM, Kalhan A (2018) Hypothyroidism during pregnancy: Controversy over screening and intervention, World J. Obstet. Gynecol. 7 (1): 1-16. doi: 10.5317/wjog.v7.i1.
23. Krajewski S, Krajewska M, Ellerby LM et al. (1999) Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc. Natl. Acad. Sci. 96 (10): 5752-5757. https://doi.org/10.1073/pnas.96.10.5752.
24. Srinivasan V, Spence DW, Pandi-Perumal SR, Brown GM, Cardinali DP (2011) Melatonin in mitochondrial dysfunction and related disorders. Int. J. Alzheimers Dis. 2011: 326320. doi: 10.4061/2011/326320.
25. Wang C, Youle RJ (2009) The role of mitochondria in apoptosis. Ann. Rev. Genet. 43: 95–118. doi:10.1146/annurev-genet-102108-134850.
26. Rebecca A. Kirkland and James L (2001) Evidence for redox regulation of cytochrome c release during programmed neuronal death: antioxidant effects of protein synthesis and caspase inhibition. J. Neurosc. 21 (6): 1949-1963; doi: https://doi.org/10.1523/JNEUROSCI.21-06-01949.2001.
27. Skulachev VP, Anisimov VN, Antonenko YN (2009) An attempt to prevent senescence: A mitochondrial approach. BBA. 1787 (5): 437-461 https://doi.org/10.1016/j.bbabio.2008.12.008.
28. Jiang X, Wang X (2004) Cytochrome C-mediated apoptosis. Ann. Rev. Biochem. 73: 87-106.
29. Tan DX, Reiter RJ (2019) Mitochondria: the birth place, battle ground and the site of melatonin metabolism in cells. Melatonin Res. 2 (1): 44-66. doi: https://doi.org/10.32794/mr11250011.
30. Beriwal N, Namgyal T, Asmaa PS, Al Quraan M (2019) Role of immune-pineal axis in neurodegenerative diseases, unraveling novel hybrid dark hormone therapies. Heliyon. 5 (1): e01190. doi: 10.1016/j.heliyon.2019.e01190.
31. Reiter RJ, Tan DX, Rosales-Corral S, Galano A, Jou MJ, Acuna-Castroviejo D (2018) Melatonin mitigates mitochondrial meltdown: interactions with SIRT3. Int. J. Mol. Sci. 19 (8): 2439. doi:10.3390/ijms19082439.
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Published
2019-12-15
How to Cite
[1]
Hidayat, M., Khaliq, S., Khurram, A. and Lone, K.P. 2019. Protective effects of melatonin on mitochondrial injury and neonatal neuron apoptosis induced by maternal hypothyroidism. Melatonin Research. 2, 4 (Dec. 2019), 42-60. DOI:https://doi.org/https://doi.org/10.32794/mr11250040.
Section
Research Articles
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