Regulation of Na<sup>+</sup>/K<sup>+</sup>-ATPase and Plasma Membrane Calcium ATPase in Brain-Gut Axis during Restraint Stress in Ageing Male Mice

Authors

  • Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala
  • Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala
  • Inter-University Centre for Evolutionary and Integrative Biology iCEIB, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala
  • Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala

DOI:

https://doi.org/10.18311/jer/2019/26218

Keywords:

Ageing, Brain-gut Axis, Na<sup> </sup>/K<sup> </sup>ATPase, Mice, PMCA, Restraint Stress

Abstract

Ageing is believed to be a continuous process that begins at conception and proceeds until death. Little is known about the response of mice to ageing and restraint stress. Therefore, in this study, BALB/c mice of different age groups (1, 2, 4 and 6 months) were subjected to restraint stress of 30 min for two consecutive days. Ion transporters being the ion homeostasis regulators of the cell, we explored the response of Na+/K+-ATPase (NKA) and Plasma Membrane Calcium ATPase (PMCA) to restraint stress, an acute stressor. We examined the activity pattern of these ATPases in mice gut (fundus and pyloric regions of the stomach, the duodenum and the jejunum) and brain (cortex, hippocampus and cerebellum) in the stressed condition. The pattern of NKA and PMCA activities showed significant shift in stressed mice that corresponds with increasing age. This differential pattern of ion transporter response in the varied regions of the brain and gut present physiological evidence for a spatio-temporal modification of ion-transporter activity during ageing and restraint stress. Overall, the present data point to a vital role of brain-gut axis in the regulation of ion homeostasis in male mice.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Allison BJ, Kaandorp JJ, Kane AD, Camm EJ, Lusby C, Cross CM, et al. Divergence of mechanistic pathways mediating cardiovascular aging and developmental programming of cardiovascular disease. FASEB J. 2016; 30(5):1968-75. https://doi.org/10.1096/fj.201500057 PMid:26932929 PMCid:PMC5036970

Drozdowski L, Thomson AB. Aging and the intestine. World J Gastroenterol WJG. 2006; 12(47):7578. https:// doi.org/10.3748/wjg.v12.i47.7578 PMid:17171784 PMCid:PMC4088037

Brust V, Schindler PM, Lewejohann L. Lifetime development of behavioural phenotype in the house mouse (Mus musculus). Front Zool. 2015; 12(S1):S17. https:// doi.org/10.1186/1742-9994-12-S1-S17 PMid:26816516 PMCid:PMC4722345

Laviola G, Macr-Fletcher S, Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev. 2003; 27(12):19-31. https://doi.org/10.1016/S0149-7634(03)00006-X

Flurkey K, Currer JM, Harrison DE. Mouse models in aging research. In: The Mouse in Biomedical Research. Elsevier; 2007. p. 637-72. https://doi.org/10.1016/B978-0123694546/50074-1

Prenderville JA, Kennedy PJ, Dinan TG, Cryan JF. Adding fuel to the fire: the impact of stress on the ageing brain. Trends Neurosci. 2015; 38(1):13-25. https://doi.org/10.1016/j.tins.2014.11.001 PMid:25705750

Pardon M-C. Stress and ageing interactions: A paradox in the context of shared etiological and physiopathological processes. Brain Res Rev. 2007; 54(2):251-73. https://doi.org/10.1016/j.brainresrev.2007.02.007 PMid:17408561

Campos AC, Fogaça MV, Aguiar DC, Guimaraes FS. Animal models of anxiety disorders and stress. Braz J Psychiatry. 2013; 35:S101-S111. https://doi.org/10.1590/1516-44462013-1139 PMid:24271222

Zhang L-N, Li J-X, Hao L, Sun Y-J, Xie Y-H, Wu S-M, et al. Crosstalk between dopamine receptors and the Na+/ K+-ATPase. Mol Med Rep. 2013; 8(5):1291-99. https://doi.org/10.3892/mmr.2013.1697 PMid:24065247

Lingrel J, Moseley AMY, Dostanic IVA, Cougnon M, He S, James P, et al. Functional roles of the α isoforms of the Na, K-ATPase. Ann N Y Acad Sci. 2003; 986(1):354-59. https://doi.org/10.1111/j.1749-6632.2003.tb07214.x PMid:12763850

Strehler EE, Caride AJ, Filoteo AG, Xiong Y, Penniston JT, Enyedi A. Plasma membrane Ca2+-ATPases as dynamic regulators of cellular calcium handling. In Sodium-Calcium Exchange and the Plasma Membrane Ca2+ATPase in Ce; Funcyion: Fifth International Conference (pp. 226-236). Ann N Y Acad Sci. 2007; 1099. https://doi.org/10.1196/annals.1387.023 PMid:17446463 PMCid:PMC3873821

Suarez AN, Hsu TM, Liu CM, Noble EE, Cortella AM, Nakamoto EM, et al. Gut vagal sensory signaling regulates hippocampus function through multi-order pathways. Nat Commun. 2018; 9(1):1-15. https://doi.org/10.1038/s41467018-04639-1 PMid:29872139 PMCid:PMC5988686

Browning KN, Travagli RA. Central nervous system control of gastrointestinal motility and secretion and modulation of gastrointestinal functions. Compr Physiol. 2011; 4(4):133968. https://doi.org/10.1002/cphy.c130055 PMid:25428846 PMCid:PMC4858318

Peter MS, Simi S. Hypoxia stress modifies Na+/K+-ATPase, H+/K+-ATPase, Na+/NH 4+-ATPase, and nkaα1 isoform expression in the brain of immune-challenged air-breathing fish. J Exp Neurosci. 2017; 11: 1179069517733732. https:// doi.org/10.1177/1179069517733732 PMid:29238219 PMCid:PMC5721975

Samuel A, Peter VS, Peter MCS. Effect of L-tryptophan feeding on brain mitochondrial ion transport in netconfined climbing perch (Anabas testudineus Bloch). J Endocrinol Reprod. 2014; 18(1):17-28.

Gulati K, Rai N, Ray A. Effects of stress on reproductive and developmental biology. In: Reproductive and Developmental Toxicology. Elsevier; 2017. p. 1063-75. https://doi.org/10.1016/B978-0-12-804239-7.00056-1

Mayer EA. Gut feelings: The emerging biology of gut-brain communication. Nat Rev Neurosci. 2011; 12(8):45366. https://doi.org/10.1038/nrn3071 PMid:21750565 PMCid:PMC3845678

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

Rezin GT, Scaini G, Gonçalves CL, Ferreira GK, Cardoso MR, Ferreira AGK, et al. Evaluation of Na+, K+-ATPase activity in the brain of young rats after acute administration of fenproporex. Braz J Psychiatry. 2014; 36(2):13842. https://doi.org/10.1590/1516-4446-2012-0956 PMid:24217638

Segovia G, Arco A del, Mora F. Environmental enrichment, prefrontal cortex, stress, and aging of the brain. J Neural Transm. 2009; 116(8):1007-16. https://doi.org/10.1007/ s00702-009-0214-0 PMid:19343473

Nilsson GE, Matthew H. R, Renshaw GMC. Low massspecific brain Na+/K+-ATPase activity in elasmobranch compared to teleost fishes: implications for the large brain size of elasmobranchs. Proc R Soc Lond B Biol Sci. 2000; 267(1450):1335-39. https://doi.org/10.1098/ rspb.2000.1147 PMid:10972129 PMCid:PMC1690671

Charmandari E, Tsigos C, Chrousos G. Endocrinology of the stress response. Annu Rev Physiol. 2005; 67(1):259-84. https://doi.org/10.1146/annurev.physiol.67.040403.120816 PMid:15709959

McFarland R, Zanjani HS, Mariani J, Vogel MW. Changes in the distribution of the α3 Na+/K+ ATPase subunit in heterozygous Lurcher Purkinje cells as a genetic model of chronic depolarization during development. Int J Cell Biol [Internet]. 2014 [cited 2020 Feb 12]; 2014. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3955620/ https://doi.org/10.1155/2014/152645 PMid:24719618 PMCid:PMC3955620

Gamaro GD, Streck EL, Matté C, Prediger ME, Wyse AT, Dalmaz C. Reduction of hippocampal Na+, K+-ATPase activity in rats subjected to an experimental model of depression. Neurochem Res. 2003; 28(9):1339-44. https:// doi.org/10.1023/A:1024988113978 PMid:12938855

Zhang LN, Su SW, Guo F, Guo HC, Shi XL, Li WY, et al. Serotonin-mediated modulation of Na+/K+ pump current in rat hippocampal CA1 pyramidal neurons. BMC Neurosci. 2012; 13(1):10. https://doi.org/10.1016/j.neuroscience.2011.12.053 https://doi.org/10.1186/14712202-13-10 PMid:22257758 PMCid:PMC3292479

Hernández-R. J, Condés-Lara M. Brain Na+/K+-ATPase regulation by serotonin and norepinephrine in normal and kindled rats. Brain Res. 1992; 593(2):239-44. https://doi.org/10.1016/0006-8993(92)91313-4

Kreydiyyeh SI. Epinephrine stimulates the Na+-K+ ATPase in isolated rat jejunal crypt cells. Life Sci. 2000; 67(11):127583. https://doi.org/10.1016/S0024-3205(00)00717-7

Saha P, Manoharan P, Arthur S, Sundaram S, Kekuda R, Sundaram U. Molecular mechanism of regulation of villus cell Na-K-ATPase in the chronically inflamed mammalian small intestine. Biochim Biophys Acta BBA-Biomembr. 2015; 1848(2):702-11. https://doi.org/10.1016/j.bbamem.2014.11.005 PMid:25462166

Lingrel JB, Williams MT, Vorhees CV, Moseley AE. Na, K-ATPase and the role of α isoforms in behavior. J Bioenerg Biomembr. 2007; 39(5-6):385-89. https://doi.org/10.1007/ s10863-007-9107-9 PMid:18044013

Hajieva P, Baeken MW, Moosmann B. The role of plasma membrane calcium ATPases (PMCAs) in neurodegenerative disorders. Neurosci Lett. 2018; 663:29-38. https://doi.org/10.1016/j.neulet.2017.09.033 PMid:29452613

Satoh E, Shimeki S. Acute restraint stress enhances calcium mobilization and glutamate exocytosis in cerebrocortical synaptosomes from mice. Neurochem Res. 2010; 35(5):693-701. https://doi.org/10.1007/s11064-009-0120-8 PMid:20069359

Bali A, Gupta S, Singh N, Jaggi AS. Implicating the role of plasma membrane localized calcium channels and exchangers in stress-induced deleterious effects. Eur J Pharmacol. 2013; 714(1):229-38. https://doi.org/10.1016/j.ejphar.2013.06.010 PMid:23796956

Stafford N, Wilson C, Oceandy D, Neyses L, Cartwright EJ. The plasma membrane calcium ATPases and their role as major new players in human disease. Physiol Rev. 2017; 97(3):1089-1125. https://doi.org/10.1152/ physrev.00028.2016 PMid:28566538

Strehler EE, Thayer SA. Evidence for a role of plasma membrane calcium pumps in neurodegenerative disease: Recent developments. Neurosci Lett. 2018; 663:39-47. https://doi.org/10.1016/j.neulet.2017.08.035 PMid:28827127 PMCid:PMC5816698

Areco V, Rivoira MA, Rodriguez V, Marchionatti AM, Carpentieri A, de Talamoni NT. Dietary and pharmacological compounds altering intestinal calcium absorption in humans and animals. Nutr Res Rev. 2015; 28(2):83-99. https://doi.org/10.1017/S0954422415000050 PMid:26466525

Liao Q-S, Du Q, Lou J, Xu J-Y, Xie R. Roles of Na+/ Ca2+ exchanger 1 in digestive system physiology and pathophysiology. World J Gastroenterol. 2019; 25(3):28799. https://doi.org/10.3748/wjg.v25.i3.287 PMid:30686898 PMCid:PMC6343099

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

Pérez AV, Picotto G, Carpentieri AR, Rivoira MA, López MEP, De Talamoni NGT. Minireview on regulation of intestinal calcium absorption. Digestion. 2008; 77(1):2234. https://doi.org/10.1159/000116623 PMid:18277073

Depke M, Fusch G, Domanska G, Geffers R, Völker U, Schuett C, et al. Hypermetabolic syndrome as a sonsequence of repeated psychological stress in mice. Endocrinology. 2008; 149(6):2714-23. https://doi.org/10.1210/en.20080038 PMid:18325986

Downloads

Published

2021-01-04

How to Cite

Thomas, A. M., Raju, L. L., Manish, K., & Subhash Peter, M. C. (2021). Regulation of Na<sup>+</sup>/K<sup>+</sup>-ATPase and Plasma Membrane Calcium ATPase in Brain-Gut Axis during Restraint Stress in Ageing Male Mice. Journal of Endocrinology and Reproduction, 23(1), 1–11. https://doi.org/10.18311/jer/2019/26218

Issue

Section

Original Research

Most read articles by the same author(s)

1 2 > >>