Impact of Restraint Stress on Mitochondrial Ion Transporter Activity in Mice Brain-Gut Regions and Gender Response to Aging

Jump To References Section

Authors

  • Department of Zoology, Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala ,IN
  • Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala ,IN
  • Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala ,IN
  • Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala ,IN
  • Department of Zoology, Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala ,IN

DOI:

https://doi.org/10.18311/jer/2019/27186

Keywords:

Aging, Brain Gut Axis, Ion Transport, Mice, Mitochondria, Restraint Stress

Abstract

The ability to respond suitably and maintain a steady state after exposure to stressors is an essential dynamic element in maintaining ion homeostasis. Besides the factors linked to the stressor itself, there are aspects intrinsic to the organisms that are pertinent to shape the stress response, such as age, gender and genetics. This study in mice analyses the functional role of mitochondria, which may affect the integrated responses to psychological stress. Mitochondria depend on a series of ion transporters to interface the communication between the cytosol and the site of energy production, which is key to the survival of the organism. Ion transporters, like mCa2+ATPase, F1F0ATPase and mH+ATPase, are the functional components of the mitochondria involved in Ca2+, H+ homeostasis and energy production. Since the process of aging starts with the birth, and ends with the death of an organism, physiological and molecular processes tend to vary throughout aging. Moreover, males and females have qualitatively different mitochondria, and only a little is known about the mitochondrial responses to stressors. Therefore, we hypothesized that mitochondrial ion transporter functions would modulate the organism's multisystemic response to psychological stress in an age-, gender- and tissue-specific manner. In this study, BALB/c mice of different age groups (4 weeks-, 8 weeks-, 16 weeks- and 24 weeks-old mice) were subjected to restraint stress of 30 minutes for two consecutive days and the ion transporter activity was quantified in the different regions of the brain (cerebrum, cerebellum and hippocampus) and the gut (duodenum of the intestine, fundus and pyloric regions of the stomach). Overall, the data indicate that in mice both gender-specific and age-specific differential sensitivities to restraint stress exist in mitochondrial ion transporter function in the brain and gut regions. This further points to a decisive interactive role of stress and sex hormones in the energetics and ion transport performance of brain-gut axis in mice.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Downloads

Published

2021-03-31

How to Cite

Raju, L. L., Thomas, A. M., Manish, K., Peter, V. S., & Subhash Peter, M. C. (2021). Impact of Restraint Stress on Mitochondrial Ion Transporter Activity in Mice Brain-Gut Regions and Gender Response to Aging. Journal of Endocrinology and Reproduction, 23(2), 65–79. https://doi.org/10.18311/jer/2019/27186

Issue

Section

Original Research

 

References

Magiakou MA, Mastorakos G, Webster E, Chrousos GP. The hypothalamic-pituitary-adrenal axis and the female reproductive system. Ann NY Acad Sci. 1997; 816(1):4256. https://doi.org/10.1111/j.17496632.1997.tb52128.x. PMid:9238254.

Novais A, Monteiro S, Roque S, Correia-Neves M, Sousa N. How age, sex and genotype shape the stress response. Neurobiol. of Stress. 2017; 6:44-56. https:// doi.org/10.1016/j.ynstr.2016.11.004. PMid:28229108 PMCid:PMC5314441.

Pardon M-C. Stress and ageing interactions: A paradox in the context of shared etiological and physiopathological processes. Brain Res. Rev. 2007; 54(2):251-273. https://doi.org/10.1016/j.brainresrev.2007.02.007. PMid:17408561.

Bale TL, Epperson CN. Sex differences and stress across the lifespan. Nat Neurosci. 2015; 18(10):1413-1420. https://doi.org/10.1038/nn.4112. PMid:26404716 PMCid:PMC4620712.

de Kloet ER, Joí«ls M, Holsboer F. Stress and the brain: From adaptation to disease. Nat. Rev. Neurosci. 2005; 6(6):463475. https://doi.org/10.1038/nrn1683. PMid:15891777.

Julio-Pieper M, Bravo JA, Aliaga E, Gotteland M. intestinal barrier dysfunction and central nervous system disorders-a controversial association. Aliment Pharmacol Ther. 2014; 40(10):1187-1201. https://doi.org/10.1111/apt.12950. PMid:25262969.

Zhang L, Song J, Bai T, Qian W, Hou X-H. Stress induces more serious barrier dysfunction in follicle-associated epithelium than villus epithelium involving mast cells and protease-activated receptor-2. Sci Rep. 2017; 7(1):4950. https://doi.org/10.1038/s41598-017-05064-y. PMid:28694438 PMCid:PMC5503989.

Peter MS, Mini VS, Bindulekha DS, Peter VS. Short-term in situ effects of prolactin and insulin onion transport in liver and intestine of freshwater climbing perch. JER. (Anabas testudineus Bloch). 2014; 18(1):47-58.

Alexander JB, Ingram GA. A comparison of five of the methods commonly used to measure protein concentrations in fish sera. J of Fish Bio. 1980; 16(2):115-122. https://doi.org/10.1111/j.1095-8649.1980.tb03691.x.

Feng-Li Lian, Moyne J, Tilbury D. Network design consideration for distributed control systems. IEEE Transac on Cont Sys Tech. 2002; 10(2):297-307. https://doi.org/10.1109/87.987076.

Picard M, McEwen BS. Psychological stress and mitochondria: A systematic review. Psychosom. Med. 2018; 80(2):141153. https://doi.org/10.1097/PSY.0000000000000545. PMid:29389736 PMCid:PMC5901654

Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R. Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene. 2008; 27(50):6407-6418. https://doi.org/10.1038/onc.2008.308. PMid:18955969 PMCid:PMC2844952.

Paupe V, Prudent J. New insights into the role of mitochondrial calcium homeostasis in cell migration. Biochem. Biophys Rese Communi. 2018; 500(1):75-86. https://doi.org/10.1016/j.bbrc.2017.05.039. PMid:28495532 PMCid:PMC5930976.

Lopes GS, Ferreira AT, Oshiro ME, Vladimirova I, Jurkiewicz NH, Jurkiewicz A, et al. Aging-related changes of intracellular Ca2+ stores and contractile response of intestinal smooth muscle. Exp. Gerontol. 2006; 41(1):55-62. https://doi.org/10.1016/j.exger.2005.10.004. PMid:16343836.

Kulish O, Wright AD, Terentjev EM. F1 rotary motor of ATP synthase is driven by the torsionally-asymmetric drive shaft. Sci Rep. 2016; 6:28180. https://doi.org/10.1038/ srep28180. PMid:27321713 PMCid:PMC4913325.

Tsakiris S, Kontopoulos AN. Time changes in Na+, K+-ATPase, Mg++-ATPase, and acetylcholinesterase activities in the rat cerebrum and cerebellum caused by stress. Pharmacol Biochem Behav. 1993; 44(2):339-342. https://doi.org/10.1016/0091-3057(93)90471-5.

Guerrieri F, Capozza G, Kalous M, Zanotti F, Drahota Z, Papa S. Age-dependent changes in the mitochondrial F0F1 ATP synthase. Arch Gerontol Geriatr. 1992; 14(3):299-308. https://doi.org/10.1016/0167-4943(92)90029-4.

Fillingame RH. Coupling H+ transport and ATP synthesis in F1F0-ATP synthases: Glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 1997; 200(2):217-24.

Chang J-C, Oude Elferink R. Role of the bicarbonateresponsive soluble adenylyl cyclase in pH sensing and metabolic regulation. Front Physiol. 2014; 5:42. https://doi.org/10.3389/fphys.2014.00042.

Lukacs G, Rotstein OD, Grinstein S. An overview of intracellular pH regulation: Role of vacuolar H+-ATPases. In: Organellar Proton-ATPases. Springer, Molecular Biology Intelligence Unit. Springer, Berlin: Heidelberg; 1995. p. 29-47. https://doi.org/10.1007/978-3-662-22265-2_2.

Nishi T, Forgac M. The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 2002; 3(2):94-103. https://doi.org/10.1038/nrm729. PMid:11836511.

Moriyama Y, Futai M. H+-ATPase, a primary pump for accumulation of neurotransmitters, is a major constituent of brain synaptic vesicles. Biochem. Biophys Res Commu. 1990; 173(1):443-448. https://doi.org/10.1016/S0006291X(05)81078-2.

Young EA. The role of gonadal steroids in hypothalamicpituitaryadrenal axis regulation. Critical Rev in Neurobio. 1995; 9(4):371-381.

Most read articles by the same author(s)

1 2 3 > >>