Rapid action of Triiodothyronine on Mitochondrial H+, Ca2+ and Mg2+-Dependent ion Transporters in Cortex, Hippocampus and Cerebellum of Restraint Mice

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Authors

  • Department of Zoology, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695 581, Kerala ,IN
  • Inter-University Centre for Evolutionary and Integrative Biology (iCEIB), School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695 581, Kerala ,IN
  • Department of Zoology, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695 581, Kerala ,IN

DOI:

https://doi.org/10.18311/jer/2019/26221

Keywords:

Brain, Mice, Mitochondrial Ca2 , H , Mg2 ATPase, Restraint Stress, Triiodothyronine

Abstract

Thyroid hormones (TH) have a multitude of actions, mainly on development and differentiation during early life and play many vital roles in almost all tissues including neuronal tissues. TH rapidly alters the mitochondrial functions both by its genomic and direct actions on mitochondrial binding sites. The functional relationship between TH and mitochondrial ion transport during stress response has not yet been elucidated in mammals so far. Here, we report a rapid in vivo action of triiodothyronine (T3) on mitochondrial ion transporter functions in the neuronal clusters of cortex, hippocampus and cerebellum of Swiss Albino mouse (Mus musculus) treated short-term with triiodothyronine (T3; 200ng g-1) for 30 min either in non-stressed or in restraint-stressed (30 min each day for 7 days). The mH+-ATPase activity in the cortex decreased to significant levels after T3 treatment in both non-stressed and restraint-stressed mice. On the contrary, the mH+-ATPase activity in the hippocampus and cerebellum increased to significant levels after T3 treatment in both non-stressed and restraint-stressed mice. The mCa2+-ATPase activity in the cortex and cerebellum decreased to significant levels after T3 treatment in both non-stressed and restraint-stressed mice. The mCa2+-ATPase activity in the hippocampus that increased to significant levels after T3 treatment, showed a reversal after restraint-stress in T3-treated mice. The mitochondrial Mg2+-ATPase activity in the cortex decreased to significant levels after T3 treatment in restraint-stressed mice. On the contrary, T3 treatment in restraint stressed mice increased to significant levels the mitochondrial Mg2+-ATPase activity in the cerebellum. The mitochondrial Mg2+-ATPase activity in the hippocampus, which increased to significant levels after T3 treatment in non-stressed mice, reversed its activity in T3-treated restraint-stressed mice. Spatial and differential action of T3 on the mitochondrial ion transporters has been found in the present study that corroborates with a rapid modulatory action of T3 on the transport of H+, Ca2+ and Mg2+ in the brain mitochondria of mice which appears to be sensitive to restraint stress.

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Published

2021-01-04

How to Cite

Simi, S., Manish, K., & Subhash Peter, M. C. (2021). Rapid action of Triiodothyronine on Mitochondrial H<sup>+</sup>, Ca<sup>2+</sup> and Mg<sup>2+</sup>-Dependent ion Transporters in Cortex, Hippocampus and Cerebellum of Restraint Mice. Journal of Endocrinology and Reproduction, 23(1), 25–36. https://doi.org/10.18311/jer/2019/26221

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References

Helmreich DL, Tylee D. Thyroid hormone regulation by stress and behavioral differences in adult male rats. Horm Behav. 2011; 60(3):284-91. https://doi.org/10.1016/j.yhbeh.2011.06.003 PMid:21689656 PMCid:PMC3148770

Weitzel JM, Iwen KA, Seitz HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol. 2003; 88(01):121-28. https://doi.org/10.1113/eph8802506 PMid:12552316

Thompson CK, Cline HT. Thyroid hormone acts locally to increase neurogenesis, neuronal differentiation, and dendritic arbor elaboration in the tadpole visual system. J Neurosci. 2016; 36(40):10356-375 https://doi.org/10.1523/JNEUROSCI.4147-15.2016 PMid:27707971 PMCid:PMC5050329

Louzada RA, Carvalho DP. Similarities and differences in the peripheral actions of thyroid hormones and their metabolites. Front Endocrinol. 2018; 9:394. https:// doi.org/10.3389/fendo.2018.00394 PMid:30072951 PMCid:PMC6060242

Mullur R, Liu Y, Brent GA. Thyroid hormone regulation of metabolism. Physiol Rev. 2014; 94(2):355-82. https:// doi.org/10.1152/physrev.00030.2013 PMid:24692351 PMCid:PMC4044302

Liu YY, Brent GA. Thyroid hormone and the brain: Mechanisms of action in development and role in protection and promotion of recovery after brain injury. Pharmacol Ther. 2018; 186:176-85. https://doi.org/10.1016/j.pharmthera.2018.01.007 PMid:29378220 PMCid:PMC5962384

Lovinger DM. Communication networks in the brain: Neurons, receptors, neurotransmitters and alcohol. Alcohol Res Health. 2008; 31(3):196-214.

Lyons DJ. Chapter 11 - Hormones and the regulation of neuronal voltage-sensing ion channels. Hormonal signaling in biology and medicine. Comprehensive Modern Endocrinology. 2020. p. 227-81. https://doi.org/10.1016/ B978-0-12-813814-4.00011-0

Peter MCS (2013) Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation. Gen Comp Endocrinol. 2013; 181:59-64. https://doi.org/10.1016/j.ygcen.2012.09.016 PMid:23063668

Sánchez O, Arnau A, Pareja M, Poch E, Ramirez I, Soley M. Acute stress-induced tissue injury in mice: differences between emotional and social stress. Cell Stress Chaperones. 2002; 7:36-46. https://doi.org/10.1379/14661268(2002)007<0036:ASITII>2.0.CO;2

Stinnett GS, Seasholtz AF. Stress and emotionality. Koob GF, Le Moal MRF, Thompson RF (eds) Encyclopedia of Behavioral Neuroscience. 2010; San Diego, CA, USA: Elsevier. 316-21. https://doi.org/10.1016/B978-0-08045396-5.00232-3

Khan AS, Peter MCS. Short-term in situ action of melatonin on ion transport in mice kept at restraint stress. J Endocrinol Reprod. 2015; 19(1):1-14. https://doi.org/10.18519/jer/2015/v19/86052

Ruszymah BH, Khalid BA. A survey of recent results concerning glycyrrhizic acid in stress and adaptation. Med J Islamic Acad Sci. 1999; 12:25-8.

Peter VS, Peter MCS. The interruption of thyroid and interrenal and the inter-hormonal interference in fish: does it promote physiologic adaptation or maladaptation? Gen Comp Endocrinol. 2011; 174:249-580. https://doi.org/10.1016/j.ygcen.2011.09.018 PMid:22001502

Shi Y, Devadas S, Greeneltch KM, Yin D, Allan MR, Zhou JN. Stressed to death: implication of lymphocyte apoptosis for psychoneuroimmunology. Brain Behav Immun. 2003; 17:S18-S26. https://doi.org/10.1016/S08891591(02)00062-4

Oishi K, Yokoi M, Maekawa S, Sodeyama C, Shiraishi T, Kondo R, Kuriyama T, Machida K. Oxidative stress and haematological changes in immobilized rats. Acta Physiol Scand. 1999; 165:65-9. https://doi.org/10.1046/j.1365201x.1999.00482.x PMid:10072099

Chen Y, Andres AL, Frotscher M, Baram TZ. Tuning synaptic transmission in the hippocampus by stress: the CRH system. Front Cell Neurosci. 2012; 6:13. https://doi.org/10.3389/fncel.2012.0001PMid:22514519 PMCid:PMC3322336

Jaggi AS, Bhatia N, Kumar N, Singh N, Anand P, Dhawan R. A review on animal models for screening potential antistress agents. Neurol Sci. 2011; 32:993-1005. https://doi.org/10.1007/s10072-011-0770-6 PMid:21927881

Santha P, Veszelka S, Hoyk Z, Meszaros M, Walter FR, Toth AE, Kiss L, Kincses A, Olah Z, Seprenyi G, Rakhely G, Der A, Pakaski M, Kalaman J, Kittel A, Deli MA. Restraint stress induced morphological changes at the blood-brain barrier in adult rats. Front Mol Neurosci. 2016; 8:88. https://doi.org/10.3389/fnmol.2015.00088 PMid:26834555 PMCid:PMC4712270

Woo H, Hong CJ, Jung S, Choe S, Yu S. Chronic restraint stress induces hippocampal memory deficits by impairing insulin signaling. Mol Brain. 2018: 11(1):37. https:// doi.org/10.1186/s13041-018-0381-8 PMid:29970188 PMCid:PMC6029109

Tarjus A, Amador C, Michea L, Jaisser F. Vascular mineralocorticoid receptor and blood pressure regulation. Curr Opin Pharmacol. 2015; 21:138-144. https://doi.org/10.1016/j.coph.2015.02.004 PMid:25733376

Smith M A. Hippocampal vulnerability to stress and aging: possible role of neurotrophic factors. Behav Brain Res. 1996; 78: 25-36. https://doi.org/10.1016/0166-4328(95)00220-0

Egeland M, Zunszain PA, Pariante CM. Molecular mechanisms in the regulation of adult neurogenesis during stress. Nat Rev Neurosci. 2015; 16:189-200. https://doi.org/10.1038/nrn3855 PMid:25790864

Cioffi F, Senese R, Lanni A, Goglia F. Thyroid hormones and mitochondria: With a brief look at derivatives and analogues. Mol Cell Endocrinol. 2013; 379:51-61. https:// doi.org/10.1016/j.mce.2013.06.006 PMid:23769708

De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R.A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature. 2011; 476:336-40. https://doi.org/10.1038/nature10230 PMid:21685888 PMCid:PMC4141877

Xu T, Pagadala V, Mueller DM. Understanding structure, function, and mutations in the mitochondrial ATP synthase. Microbial Cell. 2015; 2(4):105-25. https://doi.org/10.15698/ mic2015.04.197 PMid:25938092 PMCid:PMC4415626

Peter MCS, Lock RAC, Wendelaar Bonga SE. Evidence for an osmoregulatory role of thyroid hormones in the freshwater Mozambique tilapia, Oreochromis mossambicus. Gen Comp Endocrinol. 2000; 120:157-67. https://doi.org/10.1006/gcen.2000.7542 PMid:11078627

Fe' Raille E, Doucet A. Sodium-potassium-adenosi netriphosphate-dependent sodium transport in the kidney: hormonal control. Physiol Rev. 2001; 81:345-418. https://doi.org/10.1152/physrev.2001.81.1.345 PMid:11152761

Brini M. Ca2+ signalling in mitochondria: mechanism and role in physiology and pathology. Cell Calcium. 2003; 34:399-405. https://doi.org/10.1016/S0143-4160(03)00145-3

Chouhan AK, Ivannikov MV, Lu Z, Sugimori M, Llinas RR, Macleod GT. Cytosolic calcium coordinates mitochondrial energy metabolism with presynaptic activity. J Neurosci. 2012; 32:1233-43. https://doi. org/10.1523/JNEUROSCI.1301-11.2012 PMid:22279208 PMCid:PMC3531998

Groffen AJ, Martens S, Arazola RD, Cornelisse LN, Lozovaya N, de Jong AP, Goriounova NA, Habets RL, Takai Y, Borst JG, Brose N, Mc Mahon HT, Verhage M. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science. 2010; 327:1614-18. https://doi.org/10.1126/science.1183765 PMid:20150444 PMCid:PMC2846320

Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature. 2011; 476:341-45. https://doi.org/10.1038/nature10234 PMid:21685886 PMCid:PMC3486726

Palty R, Silverman WF, Hershfinkel M, Caporale T, Sensi SL, Parnis J, Nolte C, Fishman D, Shoshan-Barmatz V, Herrmann S, Khananshvili D, Sekler I. NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc Natl Acad Sci U S A. 2010; 107:436-41. https://doi.org/10.1073/pnas.0908099107 PMid:20018762 PMCid:PMC2806722

Bulygin VV, Vinogradov AD. Interaction of Mg2+ with FoF1 mitochondrial ATPase as related to its slow active/inactive transition. Biochem J. 1991; 276:149156. https://doi.org/10.1042/bj2760149 PMid:1828147 PMCid:PMC1151157

Syroeshkin AV, Galkin MA, Sedlov AV, Vinogradov AD. Kinetic mechanism of FoF1 mitochondrial ATPase: Mg2+ requirement for Mgâ‹…ATP hydrolysis. Biochemistry (Moscow). 1999; 64(10):1128-37.

Wang B. Analysis of ATPase activity of mitochondria intima in exercise-induced fatigue. Chem Eng Trans. 2018. p. 64

Peter MCS, Mini VS, Bindulekha DS, Peter VS. Short-term in situ effects of prolactin and insulin on ion transport in liver and intestine of freshwater climbing perch (Anabas testudineus Bloch). J Endocrinol Reprod. 2014; 18(1):4758.

Peter MCS, Leji J, Peter VS. Ambient salinity modifies the action of triiodothyronine in air-breathing fish Anabas testudineus Bloch: Effects on mitochondria-rich cell distribution, osmotic and metabolic regulations. Gen Comp Endocrinol. 2011; 171:225-31. https://doi.org/10.1016/j.ygcen.2011.01.013 PMid:21295572

Noda M. Thyroid hormone in the CNS: Contribution of neuron-glia interaction. Vitam Horm. 2018; 106:313-31. https://doi.org/10.1016/bs.vh.2017.05.005 PMid:29407440

Klingenberg M. The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta. 2008; 1778(10):1978-2021. https://doi.org/10.1016/j.bbamem.2008.04.011 PMid:18510943

Bertholet AM, Chauchani ET, Kazak L, Angelin A, Fedorenko A, Long JZ, Vidoni S, Garrity R, Cho J, Terada N, Wallace DC, Spoegelman BM, Kirichok Y. H+ transport is an integral function of the mitochondrial ADP/ATP carrier. Nature. 2019; 571(7766):515-20. https://doi.org/10.1038/ s41586-019-1400-3 PMid:31341297 PMCid:PMC6662629

Westerholz S, de Lima AD, Voigt T. Thyroid hormonedependent development of early cortical networks:

temporal specificity and the contribution of trkB and mTOR pathways. Front Cell Neurosci. 2013; 7:121. https://doi.org/10.3389/fncel.2013.00121 PMid:23964198 PMCid:PMC3734363

Losi G, Garzon G, Puia G. Nongenomic regulation of glutamatergic neurotrans mission in hippocampus by thyroid hormones. Neuroscience. 2008; 151: 155-63. https://doi.org/10.1016/j.neuroscience.2007.09.064 PMid:18065155

Incerpi S, Luly P, De Vito P, Farias RN. Short-term effects of thyroid hormone on the Na/H antiport in L-6 myoblasts: high molecular specificity for 3, 3"², 5-triiodo-l-thyronine. Endocrinology. 1998; 140:683-89. https://doi.org/10.1210/ en.140.2.683 PMid:9927294

D'Arezzo S, Incerpi S, Davis FB, Acconcia F, Marino M, Farias RN, Davis PJ. Rapid nongenomic effects of 3, 5, 3"²-triiodo-l-thyronine on the intracellular pH of L-6 myoblasts are mediated by intracellular calcium mobilization and kinase pathways. Endocrinology. 2004; 145: 5694-703. https://doi.org/10.1210/en.2004-0890 PMid:15345678

Gilbert ME, Sui L, Walker MJ, Anderson W, Thomas S, Smoller SN. Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology. 2007; 148:92-102. https://doi.org/10.1210/en.2006-0164 PMid:17008398

Westerholz S, de Lima AD, Voigt T. Regulation of early spontaneous network activity and GABAergic neurons development by thyroid hormone. Neuroscience. 2010; 168: 573-89. https://doi.org/10.1016/j.neuroscience.2010.03.039 PMid:20338226

Wiens SC, Trudeau VL. Thyroid hormone and γ-aminobutyric acid (GABA) interactions in neuroendocrine systems. Comp Biochem Physiol Part A: Mol Int Physiol. 2006; 144: 332-44. https://doi.org/10.1016/j.cbpa.2006.01.033 PMid:16527506

Kullmann D. Synaptic function. In: Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J, editors. The Hippocampus Book. Oxford University Press. 2007; 203-241.

Wheeler DW, White CM, Rees CL, Komendantov AO, Hamilton DJ, Ascoli GA. Hippocampome.org: a knowledge base of neuron types in the rodent hippocampus. eLife. 2015; 4: e09960. https://doi.org/10.7554/eLife.09960 PMid:26402459 PMCid:PMC4629441

Emptage NJ, Reid CA, Fine A. Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron. 2001; 29:197-208. https://doi.org/10.1016/S0896-6273(01)00190-8

Rusakow DA. Ca2+-dependent mechanisms of presynaptic control at central synapses. Neuroscientist. 2006; 12(4):317-326. https://doi.org/10.1177/1073858405284672 PMid:16840708 PMCid:PMC2684670

Lei J, Mariash CN, Ingbar DH. T3 increases Na, K-ATPase activity via a MAPK/ERK1/2-dependent pathway in rat adult alveolar cells. Am J Physiol. Lung Cell Mol Physiol. 2006; 294: L749-L754. https://doi.org/10.1152/ ajplung.00335.2007 PMid:18223161

Davis PJ, Davis FB, Lin HY, Mousa SA, Zhou M, Luidens MK. Translational implications of nongenomic actions of thyroid hormone initiated at its integrin receptor. Am J Physiol Endocrinol Metab. 2009; 297(6): E1238-E1246. https://doi.org/10.1152/ajpendo.00480.2009 PMid:19755667

Sakaguchi Y, Cui G, Sen L. Acute effects of thyroid hormone on inward rectifier potassium channel currents in guinea pig ventricular myocytes. Endocrinology. 1996. 137: 4744-751. https://doi.org/10.1210/en.137.11.4744 PMid:8895342

Yonkers MA, Ribera AB. Sensory sodium current requires nongenomic actions of thyroid hormone during development. J Neurophysiol. 2008; 100: 2719-725. https://doi.org/10.1152/jn.90801.2008 PMid:18799597 PMCid:PMC2585397

Zhou M, Cao JH, Pan J, Lin HY, Davis FB, Davis PJ. L-thyroxine enhances sodium channel current and synaptic transmission of rat prefrontal cortex pyramidal neurons. Immunol. Endocr Metab Agents Med Chem. 2011.

Williams PDE, Zahratka JA, Rodenbeck M, Wanamaker M, Wanamaker J, Linzie H, Bamber BA. Serotonin disinhibits a Caenorhabditis elegans sensory neuron by suppressing Ca2+-dependent negative feedback. J Neurosci. 2018; 21; 38(8): 2069-80. https://doi.org/10.1523/JNEUROSCI.1908-17.2018 PMid:29358363 PMCid:PMC5824741

Sulzer D, Cragg SJ, Rice ME. Striatal dopamine neurotransmission: Regulation of release and uptake. Basal Ganglia. 2016; 6(3):123-148. https://doi.org/10.1016/j.baga.2016.02.001 PMid:27141430 PMCid:PMC4850498

Chen BT, Patel JC, Moran KA, Rice ME. Differential calcium dependence of axonal versus somatodendritic dopamine release, with characteristics of both in the ventral tegmental area. Front Syst Neurosci. 2011; 5:39. https://doi.org/10.3389/fnsys.2011.00039 PMid:21716634 PMCid:PMC3115476

Simonides WS, Thelen MH, van der Linden CG, Muller A, van Hardeveld C. Mechanism of thyroid-hormone regulated expression of the SERCA genes in skeletal muscle: implications for thermogenesis. Biosci Rep. 2001; 21(2):139-54. https://doi.org/10.1023/A:1013692023449 PMid:11725863

Mongin AA. Disruption of ionic and cell volume homeostasis in cerebral ischemia: The perfect storm. Pathophysiology. 2007; 14(3-4):183-93. https://doi.org/10.1016/j.pathophys.2007.09.009 PMid:17961999 PMCid:PMC2196404

Mendes-De-Aguiar CB, Costa-Silva B, Alvarez-Silva M, Tasca CI, Trentin AG. Thyroid hormone mediates syndecan expression in rat neonatal cerebellum. Cell Mol Neurobiol 2008; 28: 795-801. https://doi.org/10.1007/s10571-0089260-7 PMid:18219570

Davis PJ, Davis FB, Mousa SA, Luidens MK, Lin HY. Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annu Rev Pharmacol Toxicol. 2011; 51: 99-115. https://doi.org/10.1146/annurevpharmtox010510-100512 PMid:20868274

Kundu S, Ray A K. Thyroid hormone homeostasis in adult mammalian brain: A novel mechanism for functional preservation of cerebral T3 content during initial peripheral hypothyroidism. Al Ameen J Med Sci. 2010; 3(1):5-20.

Sarkar PK, Ray AK. Involvement of L-triiodothyronine in acetylcholine metabolism in adult rat cerebrocortical synaptosomes. Horm Metab Res. 2001; 33:270-75. https:// doi.org/10.1055/s-2001-15120 PMid:11440272

Chakrabarti N, Ray AK. Stimulation of Ca2+/Mg2+-ATPase activity in adult rat cerebrocortical synaptosomes by 3-5-3'-L-triiodothyronine. Neurosci Res Commun. 2002; 31:193-201 https://doi.org/10.1002/nrc.10052

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