Journal of Endocrinology and Reproduction

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In Vivo Action of Nitric Oxide Donor Sodium Nitroprusside (SNP) on Mitochondrial Ion Transporter Function in Brain Segments of Immersion-Stressed Air-Breathing Fish (Anabas testudineus Bloch)


Affiliations
1 Department of Zoology, Inter-University Centre for Evolutionary and Integrative Biology School of Life Science, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala, India
2 Inter-University Centre for Evolutionary and Integrative Biology School of Life Science, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala, India
     

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The neuronal circuitries of brain and the corresponding ion transporters contribute to the maintenance of ion homeostasis in fish brain. The sensitivity of these neuronal clusters in response to environmental clues brings neural plasticity and subsequent regulation of stress acclimation. Nitric oxide (NO), a gasotransmitter, is involved in ion transport in many peripheral tissues of fishes including air-breathing fish. However, the role of NO in mitochondrial ion transporter activity has not yet been investigated in fish brain. We, therefore, investigated the short-term in vivo action of a NO donor, Sodium Nitro-Prusside (SNP), on mitochondrial ion transporters such as H+- Ca2+- and Mg2+-dependent ATPases in brain segments such as Prosen-Cephalon (PC), Mesen-Cephalon (MC) and Meten-Cephalon (MeC) of immersion-stressed Anabas testudineus. Intraperitoneal injection of SNP for 30 min lowered the activities of bafilomycin-sensitive H+ATPase and vanadate sensitive Ca2+ATPase in PC, whereas in MeC, these transporters showed significant rise in activities after SNP treatment. The oligomycin-sensitive Mg2+ATPase activity showed a significant decrease in PC and MC of brain after SNP treatment in non-stressed fish. Induction of stress by water immersion altered the activities of these ion transporter activities. However, the treatment of SNP in immersed fish showed recovery of the immersion-induced modulation in the activities of these mitochondrial ion transporters. Our data, thus, provide evidence for a decisive role of NO in the recovery process of mitochondrial ion transporters function during immersion stress, confirming a direct differential role of NO in mitochondrial ion homeostasis in teleost brain.

Keywords

Immersion-Stress, Nitric Oxide, Sodium Nitroprusside, Ca2+-ATPase, H+-ATPase, Mg2+-ATPase
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  • Wendelaar Bonga SE. The stress response in fish. Physiol Rev. 1997; 77:591-625. https://doi.org/10.1152/physrev.1997.77.3.591. PMid:9234959.

  • Peter MCS. The role of thyroid hormones in stress response of fish. Gen Comp Endocrinol. 2011; 172:198-210. https://doi.org/10.1016/j.ygcen.2011.02.023. PMid:21362420.

  • 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; 174:249-258. https://doi.org/10.1016/j.ygcen.2011.09.018. PMid:22001502.

  • Peter MCS. 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.

  • Zupanc GKH, Lamprecht J. Towards a cellular understanding of motivation: structural reorganization and biochemical switching as key mechanisms of behavioral plasticity. Ethology. 2000; 106:467-477. https://doi.org/10.1046/j.1439-0310.2000.00546.x.

  • Duman RS. Depression: a case of neuronal life and death? Biol Psych. 2004; 56: 140-145. https://doi.org/10.1016/j.biopsych.2004.02.033. PMid:15271581.

  • Shepherd JD, Huganir RL. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol. 2007; 23:613-643. https://doi.org/10.1146/annurev.cellbio.23.090506.123516. PMid:17506699.

  • Greer PL, Greenberg ME. From synapse to nucleus: Calcium-dependent gene transcription in the control of synapse development and function. Neuron. 2008; 59:846-860. https://doi.org/10.1016/j.neuron.2008.09.002. PMid:18817726.

  • Shah MM, Hammond RS, Hoffman DA. Dendritic ion channel trafficking and plasticity. Trends Neurosci. 2010; 33:307-316. https://doi.org/10.1016/j.tins.2010.03.002. PMid:20363038 PMCid:PMC2902701.

  • Todorova V, Blokland A. Mitochondria and synaptic plasticity in the mature and aging nervous system. Curr Neuropharmacol. 2017; 15(1):166-173. https://doi.org/1 0.2174/1570159X14666160414111821. PMid:27075203 PMCid:PMC5327446.

  • Nicholls DG, Budd SL. Mitochondria and neuronal survival. Physiol Rev. 2000; 80:315-360. https://doi.org/10.1152/ physrev.2000.80.1.315. PMid:10617771.

  • Toescu EC. Mitochondria and Ca2+ signaling. J Cell Mol Med. 2000; 4:164-175. https://doi.org/10.1016/j.ceca.2005.06.011. PMid:16087232.

  • Cheng A, Hou Y, Mattson MP. Mitochondria and neuroplasticity. ASN Neuro. 2010; 2(5):e00045. https://doi.org/10.1016/j.ehj.2014.04.004.

  • Picard M, McEwen BS, Epel ES, Sandi C. An energetic view of stress: focus on mitochondria. Front Neuroendocrinol. 2018; 49:72-85. https://doi.org/10.1016/j.yfrne.2018.01.001. PMid:29339091 PMCid:PMC5964020.

  • Peter MCS, Simi S. Hypoxia stress modifies Na+/ K+ATPase, H+/K+ATPase, Na+/NH4+ ATPase and nkaα1 isoform expression in brain of immune-challenged airbreathing fish. J Exp Neurosci. 2017; 11:1-8. https:// doi.org/10.1177/1179069517733732. PMid: 29238219 PMCid:PMC5721975.

  • Džoljić E, Grabatinić I, Kostić V. Why is nitric oxide important for our brain? Funct Neurol. 2015; 30:159163. https://doi.org/10.11138/FNeur/2015.30.3.159. PMid:26910176 PMCid:PMC4610750.

  • Esch T, Stefano GB, Fricchione GL, Benson H. The role of stress in neurodegenrative diseases and mental disorders. Neuro Endocrinol Lett. 2002; 23(3):199-208. https://doi.org/10.1177/15257401020230040402.

  • Kumar A, Chanana P. Role of nitric oxide in stress-induced anxiety: From pathophysiology to therapeutic target. Vitam Horm. 2017; 103: 147-167. https://doi.org/10.1016/ bs.vh.2016.09.004. PMid:28061969.

  • Bondarenko ON, Bondarenko NA, Malyshev II, Manukhina EB. Anti-stress effect of nitric oxide. Izv Akad Nauk Ser Biol. 2001; 4:459-466.

  • Masood A, Banerjee B, Vijayan VK, Ray A. Modulation of stress-induced neurobehavioral changes by nitric oxide in rats. Eur J Pharmacol. 2003; 458:135-139. https://doi.org/10.1016/S0014-2999(02)02688-2.

  • Bolaños JP, Peuchen S, Heales SJ, Land JM, Clark JB. Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochem. 1994; 63:910916. https://doi.org/10.1046/j.1471-4159.1994.63030910.x. PMid:7519665.

  • Baud O, Li J, Zhang Y, Neve RL, Volpe JJ, Rosenberg PA. Nitric oxide-induced cell death in developing oligodendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eur J Neurosci. 2004; 20:1713-1726. https://doi.org/10.1111/j.14609568.2004.03616.x. PMid:15379992.

  • Hashemy SI, Johansson C, Berndt C, Lillig CH, Holmgren A. Oxidation and S-nitrosylation of cysteines in human cytosolic and mitochondrial glutaredoxins: Effects on structure and activity. J Biol Chem. 2007; 282:1442814436. https://doi.org/10.1074/jbc.M700927200. PMid:17355958.

  • Peter MCS, Rejitha V, Dilip DG. Handling of ferric iron by branchial and intestinal epithelia of climbing perch (Anabas testudineus Bloch). Indian J Exp Biol. 2007; 45:896-900.

  • Anupriya S, 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; 1:17-28. https://doi.org/10.1155/2014/476798.

  • Sørensen C, Johansen IB, Øverli Ø. Neural plasticity and stress coping in teleost fishes. Gen Comp Endocrinol. 2013; 181:25-34. https://doi.org/10.1016/j.ygcen.2012.12.003. PMid:23274407.

  • Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AMG. Nitric oxide in the central nervous system: Neuroprotection versus neurotoxicity. Nat Rev Neurosci. 2007; 8(10):766-75. https://doi.org/10.1038/ nrn2214. PMid:17882254.

  • Snelling R, Nicholls D. Calcium efflux and cycling across the synaptosomal plasma membrane. J Biochem. 1985; 226:225-231. https://doi.org/10.1042/bj2260225. PMid:3977866 PMCid:PMC1144696.

  • Neher E, Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron. 2008; 59:861-872. https://doi.org/10.1016/j.neuron.2008.08.019. PMid:18817727.

  • Spitzer NC, Kingston PA, Manning TJ, Conklin MW. Outside and in: Development of neuronal excitability. Curr Opin Neurobiol. 2002; 12:315-323. https://doi.org/10.1016/ S0959-4388(02)00330-6.

  • Mishra OP, Delivoria-Papadopoulos M. Nitric oxidemediated Ca++-influx in neuronal nuclei and cortical

  • synaptosomes of normoxic and hypoxic newborn piglets. Neurosci. Lett. 2002; 318:93-97. https://doi.org/10.1016/ S0304-3940(01)02484-3.

  • Zanelli SA, Numagami Y, McGowan JE, Mishra OP, Delivoria-Papadopoulos M. NMDA receptor-mediated calcium influx in cerebral cortical synaptosomes of the hypoxic guinea pig fetus. Neurochem Res. 1999; 24:437-446. https://doi.org/10.1023/A:1020950019986. PMid:10215519.

  • Rizzuto R, De Stefani D, Raffaello A, Mammucari C: Mitochondria as sensors and regulators of calcium signaling. Mol Cell Biol. 2012; 13:566-578. https://doi.org/10.1038/nrm3412. PMid:22850819.

  • Yamagata SK, Parsons SM. Cholinergic synaptic vesicles contain a V-type and a P-type ATPase. J Neurochem. 1989; 53(5):1354-62. https://doi.org/10.1111/j.1471-4159.1989.tb08525.x. PMid:2552014.

  • Moriyama Y, Maeda M, Futai M. The role of V-ATPase in neuronal and endocrine systems. J Exp Biol. 1992; 172:171-178.

  • Wolosker H, Reis M, Assreuy J, de Meis L. Inhibition of glutamate uptake and proton pumping in synaptic vesicles by S-nitrosylation. J Neurochem. 1996; 66:19438. https://doi.org/10.1046/j.1471-4159.1996.66051943.x. PMid:8780021.

  • Moriyama Y, Futai M. H+ATPase, a primary pump for accumulation of neurotransmitters, is a major constituent of brain synaptic vesicles. Biochem Biophys Res Commun. 1990; 173:443-446. https://doi.org/10.1016/S0006291X(05)81078-2.

  • Nelson N. Structure and pharmacology of the protonATPases. Trends Pharmacol Sci. 1991; 12:71-75. https:// doi.org/10.1016/0165-6147(91)90501-I.

  • Torlinska T, Grochowalska A. Age-related changes of Na+, K+, Ca2+-ATPase and Mg2+ ATPase activities in rat brain synaptosomes. J Physiol Pharmacol. 2004; 55:457-465.

  • Wang Y, Ze J, Jing C. Effect of acupuncture on NO, NOS and Ca2+-Mg2+-ATPase activity in brain tissue of subacute aging rats induced by D-galactose. J Acupunct Tuina Sci. 2012; 10(3):146-149. https://doi.org/10.1007/s11726-012-0591-z.

  • Matsuda H. Magnesium gating of the inwardly rectifying K+ channel. Annu Rev Physiol. 1991; 53:289-298. https://doi.org/10.1146/annurev.ph.53.030191.001445. PMid:2042964.

  • Esplugues JV. NO as a signalling molecule in the nervous system. Br J Pharmacol. 2002; 135:1079-1095. https://doi.org/10.1038/sj.bjp.0704569. PMid:11877313 PMCid:PMC1573233.


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  • In Vivo Action of Nitric Oxide Donor Sodium Nitroprusside (SNP) on Mitochondrial Ion Transporter Function in Brain Segments of Immersion-Stressed Air-Breathing Fish (Anabas testudineus Bloch)

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Authors

R. Gayathry
Department of Zoology, Inter-University Centre for Evolutionary and Integrative Biology School of Life Science, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala, India
Valsa S. Peter
Inter-University Centre for Evolutionary and Integrative Biology School of Life Science, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala, India
M. C. Subhash Peter
Department of Zoology, Inter-University Centre for Evolutionary and Integrative Biology School of Life Science, University of Kerala, Kariavattom, Thiruvananthapuram - 695581, Kerala, India

Abstract


The neuronal circuitries of brain and the corresponding ion transporters contribute to the maintenance of ion homeostasis in fish brain. The sensitivity of these neuronal clusters in response to environmental clues brings neural plasticity and subsequent regulation of stress acclimation. Nitric oxide (NO), a gasotransmitter, is involved in ion transport in many peripheral tissues of fishes including air-breathing fish. However, the role of NO in mitochondrial ion transporter activity has not yet been investigated in fish brain. We, therefore, investigated the short-term in vivo action of a NO donor, Sodium Nitro-Prusside (SNP), on mitochondrial ion transporters such as H+- Ca2+- and Mg2+-dependent ATPases in brain segments such as Prosen-Cephalon (PC), Mesen-Cephalon (MC) and Meten-Cephalon (MeC) of immersion-stressed Anabas testudineus. Intraperitoneal injection of SNP for 30 min lowered the activities of bafilomycin-sensitive H+ATPase and vanadate sensitive Ca2+ATPase in PC, whereas in MeC, these transporters showed significant rise in activities after SNP treatment. The oligomycin-sensitive Mg2+ATPase activity showed a significant decrease in PC and MC of brain after SNP treatment in non-stressed fish. Induction of stress by water immersion altered the activities of these ion transporter activities. However, the treatment of SNP in immersed fish showed recovery of the immersion-induced modulation in the activities of these mitochondrial ion transporters. Our data, thus, provide evidence for a decisive role of NO in the recovery process of mitochondrial ion transporters function during immersion stress, confirming a direct differential role of NO in mitochondrial ion homeostasis in teleost brain.

Keywords


Immersion-Stress, Nitric Oxide, Sodium Nitroprusside, Ca2+-ATPase, H+-ATPase, Mg2+-ATPase

References





DOI: https://doi.org/10.18311/jer%2F2019%2F27185